KAUST Discovery - Issue 9 by KAUST

ISSUE 9 / SPRING SEMESTER 2020

U SING A N EMBRYONIC PA U S E T O S AV E T HE D AT E

T IN Y T W E A K S F OR BIG W IN S IN S OL A R CEL L S P.15

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K EEPING SE CR E T S PER F E C T LY SAFE WITH NE W OP T IC A L CHIP S P.31

FOOD FOR THE FUTURE

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A LETTER

FROM THE VICE PRESIDENT FOR RESE ARCH

Dear Reader, Forecasts indicate that by 2050, the global human population will reach 10 billion, a situation that will create significant challenges for all of us. Not only must we grow more food to feed additional people, we also must do it sustainably on a warming Earth. This issue of KAUST Discovery highlights some of the work that our researchers are doing to address the “How to feed 10 billion?” question, which aligns with one of KAUST’s four founding research pillars— food. In fact, to find some of the answers to this question, we recently launched our Center for Desert Agriculture. The members of the Center are taking a “systems” approach to agriculture that simultaneously optimizes biological productivity and minimizes water and energy consumption, nutrient inputs, environmental impact and cost. There is no question that it will take many minds and a healthy serving of ideas to find the multifaceted solutions that we need to address this grand challenge. Throughout our feature section, we share with you how our researchers are working individually and collaboratively on these solutions. Specifically, in our feature story, you will read about how Rod Wing is domesticating a wild relative of rice that can grow in saltwater, how Mark Tester is breeding quinoa as an alternative staple crop in countries facing issues of food security, how Ikram Blilou is investigating date palm genomes to identify how these plants thrive in arid soils and high desert temperatures, and how Salim Al-Babili is minimizing the annual crop losses that exceed US$7 billion caused by an invasive parasitic plant called Striga. Meanwhile, Matthew McCabe is working with the Ministry of Environment, Water and Agriculture to map agricultural water use throughout the Kingdom to better understand and thereby start to sustainably manage its use. From the energy component of this foodwater-energy nexus, addressed previously in

“T h i s i s s u e of KAUST

Discovery highlights some of the work that our re searche rs are doing to address the ‘How to feed 10 billion?’ q u e s t i o n .”

issue six, you can read about materials scientist Stefaan De Wolf ’s “Tiny tweaks for big wins in solar cells” to learn how he and his group in the KAUST Solar Center are working hard to achieve better-performing, reliable and cost-competitive, perovskite-based solar cells. On a different note, we also look at electrical engineer Andrea Fratalocchi’s research that seeks to put cyberhackers out of business in a story entitled “Keeping secrets perfectly safe with new optical chips.” He and his team are using chaos in optical networks to create a scattering structure that could prevent an attacker from reproducing or accessing any exchanged information. We are very excited that Saudi Arabia will hold the presidency for this year’s G20 Summit. As an institution, we support the agenda of the Summit, “Realizing Opportunities of the 21 st Century for All,” and we believe that our vision and mission are directly aligned with the three key aims of the presidency: Empowering People, Safeguarding the Planet and Shaping New Frontiers. Moreover, we are enthusiastic to host the group of leaders who comprise the S20 branch of the Summit—the engagement group that represents the science community—on our campus. This will be a unique opportunity to share our campus and research environment with an international group of policy makers who will help to shape our future environment. Toward the University’s mission to enhance the welfare of society, we recently added two new initiatives, KAUST Smart Health and KAUST Artificial Intelligence. To learn more about the research in these areas and others, I invite you to visit the KAUST Discovery website—discovery.kaust.edu. sa—frequently and to sign up to receive our fortnightly newsletter. Professor Donal D. C. Bradley Vice President for Research

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KAUST SCIENTISTS PERFORM GENOME SEQUENCING TO IDENTIFY DESIRABLE PLANT TRAITS, such as salt, drought and disease tolerance, for transfer into a target crop plant using genome editing.

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CONTENTS /SPRING SEMESTER 2020

CLEAN EN V IRO N M EN T

A LT ER N AT I V E F U EL S

E X P L O R IN G T HE R ED S E A

N OV EL M AT ER I A L S

24 LIGANDS STABILIZE NANOCLUSTERS TO MAKE THEM BRIGHTER

Large cylindrical ligands increase stability and enhance light emission of silver nanoclusters.

25 CATALYST SWITCHING MEANS FOUR BECOME ONE 11 BUILDING APPROACH FOR OPTOELECTRONICS STACKS UP

6 PORE RESULTS FROM WASTE PLASTIC Discarded PET bottles could find a new life in the chemical industry.

8 A BREATH OF FRESH INFORMATION TO HELP DIAGNOSIS

A communications concept could pinpoint a person infected with a deadly, contagious virus in the middle of a crowded airport.

9 A COOL ALTERNATIVE TO AIR CONDITIONING

An inexpensive passive cooling technology could be used to decrease temperatures in buildings in cities, reducing energy consumption.

10 EXPANDING THE SCALE OF DANGEROUS WEATHER PREDICTION A more accurate and efficient method of capturing the local factors that lead to extreme rainfall enables better flood prediction across larger regions.

A precise method for stacking semiconductor thin films enhances optoelectronic device performance using quantum effects.

12 CHEMICAL ENLIGHTENMENT BEHIND REFLECTED SHOCKWAVES Studying the wake of reflected shockwaves reveals the cascade of chemical reactions involved in combustion processes.

13 BENCHMARKS TO BETTER CATCH THE SUN

Simulations unveil efficiency targets and design rules to maximize the conversion of light into electricity using organic solar cells.

14 FLEXIBLE THINKING ON SILICON SOLAR CELLS

Combining silicon with a highly elastic polymer backing produces solar cells that have record-breaking stretchability and high efficiency.

15 TINY TWEAKS FOR BIG WINS IN SOLAR CELLS

Changes in composition are shown to affect light-harvesting layer crystallization and perovskite solar cell efficiency.

16 SEAWEED SINKS DEEP, TAKING CARBON WITH IT

Macroalgae is shown to be a major global contributor to carbon sequestration.

18 GIANT CLAMS TRAP MARINE PLASTICS

Microplastics in the water column are ingested by clams and become attached to their shells.

20 CORALS TAKE CONTROL OF NITROGEN RECYCLING

Corals use sugar from their symbiotic algal partners to control them by recycling nitrogen from their own ammonium waste.

23 CHANGING HOW WE PREDICT CORAL BLEACHING

A remote sensing algorithm offers better predictions of Red Sea coral bleaching and can be fine-tuned for use in other tropical marine ecosystems.

Catalyst switching strategy is the key step in the production of a four-component crystalline tetrablock quarterpolymer.

26 BABY STEPS FOR TRANSPARENT ELECTRONICS

Stretchy, see-through silver nanowire sheets combine optical transparency with excellent electrical conductivity.

28 QUANTUM DESTABILIZATION OF A WATER SANDWICH

When a thin layer of water is squeezed between two hydrophobic surfaces, the laws of classical physics break down.

29 MAGNETIC SKIN ENSURES THE FORCE IS WITH YOU

A magnetic skin that is safe and comfortable to wear could open the door to a wide range of wireless, remotely controlled applications.

31 PATTERNED OPTICAL CHIPS KEEP SECRETS PERFECTLY SAFE

Chaos could help put cyberhackers out of business with a patterned silicon chip that will be uncrackable even in the future.

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CONTENTS / SPRING SEMESTER 2020

V I S UA L IZ IN G S C IEN C E

F E AT U R E

G EN E T W E A K IN G

49 PUSHING PEROVSKITE SOLAR STABILITY

Solar perovskite materials could be spiked with organic cation dopants to suppress decomposition and degradation.

50 SMART REACTIONS THROUGH ONLINE DESIGN OF CATALYTIC POCKETS 32 FOOD FOR THE FUTURE

KAUST researchers are combining their efforts to improve food security sustainably.

36 FARMING IN THE DESERT A multidisciplinary effort for sustainable agriculture.

38 RISING UP TO THE CHALLENGE OF FEEDING THE WORLD SUSTAINABLY

The world’s food system is facing increasing pressures, including climate change, a much larger number of people to feed, and greater political instability.

39 DATE PALMS PICKY ABOUT BACTERIAL PARTNERS

Cultivated date palms have co-evolved with desert bacteria for so long that their roots attract the microbes that provide the best chance for a long and healthy life.

40 STRIGA INFESTATION

Striga hermonthica, also known as “purple witchweed,” is an invasive parasitic plant that siphons off water and nutrients from the host crop for its own growth.

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42 CONFERRING LEAF RUST RESISTANCE IN CEREAL CROPS

Identifying genes that confer resistance to leaf rust infections could help generate durably resistant cereal crops.

44 USING AN EMBRYONIC PAUSE TO SAVE THE DATE

A date palm seedling can pause its development to boost its resilience before emerging into the harsh desert environment.

46 TESTING BARLEY’S SALT TOLERANCE IS A NUMBERS GAME

Factors influencing the tolerance of barley to saline soils have been uncovered using an advanced robust statistical technique.

Mapping the three-dimensional structure of catalytic centers helps to design new and improved catalysts.

51 AI USES YOUR IMAGINATION

The psychology of human creativity helps artificial intelligence imagine the unseen.

52 SPOTTING CANCER’S GREASY FINGERPRINTS

Laser-based microscopes can tune into multiple biomolecular signatures found in cancer cells.

54 MASTERING A PRICKLY PROBLEM IN FERROFLUIDS

Computer simulation accurately captures the beguiling motion of a liquid magnetic material.

55 EPILEPSY STUDY SHOWS THE SHAPE OF THINGS TO COME

Pyramidal graphs resulting from statistical analyses of EEG recordings can improve our understanding of epileptic seizures.

56 GLOWING RESULTS FOR SINGLE-MOLECULE IMAGING

New experimental insights allow researchers to probe protein-DNA interactions with greater precision.

58 AI REVEALS NATURE OF RNA-PROTEIN INTERACTIONS

A deep learning tool could help in structure-based drug discovery.

59 TURNING UP THE HEAT ON PATHOGENIC BACTERIA Protein found in gut-dwelling pathogens changes shape under human body temperatures, leading to toxins responsible for diarrheal disease.

60 REGULATOR OF PLANT IMMUNITY TAGGED

Discovery of signaling intermediary could lead to more pest-resistant crops.

62 CHLORINE COULD INCREASE ANTIMICROBIAL RESISTANCE Ultraviolet light could thwart antimicrobial resistance by damaging DNA material in wastewater.

63 ARGONAUTE PROTEINS HELP FINE-TUNE GENE EXPRESSION A protein, with a name reminiscent of legendary Greek sailors, has an unexpected role inside the human nucleus.

64 DATABASE TO SUPPORT INFECTIOUS DISEASE RESEARCH

Linking disease pathogens to clinical signs and symptoms through a database could support research into the molecular mechanisms of infectious diseases.

CONTENTS /SPRING SEMESTER 2020

ISSUE 9 / SPRING SEMESTER 2020

U SING A N EMBRYONIC PAU SE T O S AV E T HE D AT E

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ABOUT THE COVER

The cover image shows an early stage of date palm development from seed. At this stage, the whole seedling is hidden inside the multilayered root-like structure. The fully developed root can be seen at the bottom of the image while leaves are about to emerge from a fissure. Date palms are known to employ remote germination, a method that allows the whole seedling (root and shoot) to remain protected under the soil, pausing their development as a strategy to escape predators and to wait for favorable growth conditions. Understanding desert adaptations, such as the remote germination of the date palm, can help scientists to design strategies to help growers cultivate crops in an increasingly arid landscape. We chose to feature a date palm on the cover of this issue dedicated to “Food for the future” because of the considerable cultural and economic value of this plant for the Middle East and its potential to improve food security in arid regions. Here, the seedling signifies the potential of scientific exploration to propagate food for the future. For the full story on date palm development, read “Using an embryonic pause to save the date” on page 44.

If you would like to update your information, send us an email at discovery@kaust.edu.sa.

EDITORIAL COMMITTEE Pierre Magistretti Dean, Biological and Environmental Science and Engineering Division

MANAGING EDITOR Carolyn Unck

Mootaz Elnozahy Dean, Computer, Electrical and Mathematical Sciences and Engineering Division

EDITORIAL TEAM Carmen Denman Virginia Unkefer

GRAPHICS CONSULTANT Xavier Pita

Magnus Rueping Professor, Chemical Science Physical Science and Engineering Division

ILLUSTRATIONS AND PHOTOGRAPHY Helmy Alsagaff Heno Hwang Anastasia Khrenova Xavier Pita

KAUST DISCOVERY is published with King Abdullah University of Science and Technology (KAUST) by the Partnership and Custom Media Unit of Nature Research, part of Springer Nature. King Abdullah University of Science and Technology (KAUST) Thuwal 239556900 – Kingdom of Saudi Arabia. Email: discovery@kaust.edu.sa

O N T HE C OV ER

TINY TWEAKS FOR BIG WINS IN SOLAR CELLS

KEEPING SECRETS PERFECTLY SAFE WITH NEW OPTICAL CHIPS

USING AN EMBRYONIC PAUSE TO SAVE THE DATE

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Bruno Pulido tests the efficiency of the teamâ&#x20AC;&#x2122;s synthetic membrane.

PORE RESULTS FROM WASTE PLASTIC

Discarded PET bottles could find a new life in the chemical industry.

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In a world that seems to be drowning in plastic bottles, recycling this waste into useful materials would help to reduce its environmental impact. Researchers have now invented a way to turn plastic bottles into porous membranes that could be used as molecular filters in the chemical industry. Roughly 40 percent of the energy used by the chemical industry goes into separating and purifying chemicals in heat-intensive processes, such as distillation and crystallization. Using porous membranes to separate molecules from liquids could dramatically reduce that

CLEAN ENVIRONMENT

30% of PET is used in the food industry, including single-use plastic bottles.

“M e m b ra n e s could be used as a support for thin layers of o t h e r f i l t ra t i o n m a t e r i a l s .”

energy consumption. But most conventional membranes are not robust enough to withstand the sort of solvents used in industry, and alternative ceramic membranes tend to be very expensive. The KAUST team turned instead to recycled poly (ethylene terephthalate) (PET). “PET is mechanically and chemically robust, so it could be used in filtration and purification processes that require sterilization or cleaning with acids or bleach,”, says recent KAUST graduate Bruno Pulido. In 2016, global production of PET reached 50 million

tons, accounting for about nine percent of total plastic production. Roughly 30 percent of PET is used in the food industry, including single-use plastic bottles. PET is typically “downcycled” into lower-value products, such as clothing fabrics, so converting it into higher-value filtration membranes could provide a strong economic incentive to improve recycling rates. To create their membranes, the researches dissolved the PET and then used a different solvent to make the PET solid again, this time in the shape of a membrane instead of a bottle. The team tested a wide range of different processing conditions and solvents and used an additive called poly (ethylene glycol) (PEG) to help form pores within the PET membranes. Changing the concentration and size of the PEG molecules helped to control the number and size of pores within the membrane, and thus fine tuned its filtration properties. After optimizing this process, the team measured how easily liquid flowed through the membranes and how well the membranes separate molecules of different sizes. The best membranes had pore sizes that ranged from 35 to 100 nanometers wide, with pores covering up to 10 percent of the membrane’s area: they also performed well at 100 degrees Celsius. Pulido says that the membranes could be used as a support for thin layers of other filtration materials, such as those found in reverse osmosis membranes. “We’re also working on the development of PET hollow fibers, a type of membrane with additional advantages over flat membranes,” he adds. Pulido, B.A., Habboub, O., Aristizabal, S.L., Szekely, G. & Nunes, S.P. Recycled Poly(ethylene terephthalate) for high temperature solvent resistant membranes. ACS Applied Polymer Materials 9, 23792387 (2019).

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CLEAN ENVIRONMENT even larger degree of freedom for real-life applications, such as those needed to monitor patients under quarantine. The team is now establishing multi-

“A c o m m u n i c a tion system using inhaled and ex h a l e d b r e a t h , where the inforOsama Amin discusses the system architecture with advisors Basem Shihada (left) and MohamedSlim Alouini (right).

mation is carried

A BREATH OF FRESH INFORMATION TO HELP DIAGNOSIS

i n m o l e c u l e s .”

A communications concept could pinpoint a person infected with a deadly, contagious virus in the middle of a crowded airport. Human breath carries a breadth of information, and now this information has been harnessed by KAUST researchers Osama Amin, Mohamed-Slim Alouini and Basem Shihada working with Maryam Khalid and Sajid Ahmed at Information Technology University, Pakistan. Since the late 18th century, scientists and inventors have been developing technology to enhance human telecommunication. More recently, there has been hype around multidimensional media, which has prompted researchers to investigate ways to add other senses, such as smell, touch and taste, to the traditional senses of sound and sight. Scientists have already found ways to extract information about the human body from breath. The breathalyzer, which estimates blood-alcohol levels, was invented in the 1950s. More recently, clinicians have been using breath samples collected from patients to detect viruses, like human influenza, or even to diagnose cancers, like

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breast and lung tumors. Almost 1,000 volatile organic compounds have so far been identified in healthy human breath; these compounds vary on health, age, diet, gender, body fat, height and lifestyle. The team envisions an even broader concept. They have already designed a system architecture that can theoretically detect a person infected with a virus in the midst of a crowded area, such as an airport. “Our idea is to construct a communication system using inhaled and exhaled breath, where the information is carried in molecules,” explains Amin. Constructing such a breath communication system will open the door to a new generation of wireless body networks, he explains. These are the communications systems used by medical practitioners, for example, to wirelessly monitor health using wearable and implanted sensors that can communicate information to a remote device. A breath communication system will not replace this sort of setup, but it can offer an

disciplinary collaborations with experts in many fields to define the best communication channel models that can be used for this approach. They are asking many questions: What kinds of information can be exchanged? What types of molecular compounds would be introduced into the system to interact with the human body? What types of sensors and detectors are needed to send and receive information? And what security and privacy concerns need to be addressed? The team is also using the information that can be compiled from exhaled breath to teach machine learning algorithms how to monitor human health, measure physical activities, and even monitor a person’s psychological status. These algorithms could then be used together with sensors in future cell phones, Amin says. “Just like we’re training cell phones to recognize signatures, voices and people’s faces, breath training could be used to identify individuals and to monitor their overall state of wellbeing.” Khalid, M., Amin, O., Ahmed, S., Shihada, B. & Alouini, M.–S. Communication through breath: Aerosol transmission. IEEE Communications Magazine 57, 33-39 (2019).

CLEAN ENVIRONMENT

A COOL ALTERNATIVE TO AIR CONDITIONING

An inexpensive passive cooling technology could be used to decrease temperatures in buildings in cities, reducing energy consumption. A low-cost passive cooling technology made from a polymer film could be used to passively cool buildings in metropolitan areas, avoiding the need for electricity. Modern air conditioning systems consume significant amounts of energy to cool buildings during the daytime, generating substantial amounts of greenhouse gases responsible for climate change. For example, air conditioning accounts for around 15 percent of total primary energy consumption in the United States and can be as high as 70 percent in extremely hot countries, such as Saudi Arabia. Technologies that use radiative cooling to control the temperature of buildings, such as planar multilayered photonic films and hybrid metamaterial films, are attracting considerable attention because they do not use electricity; however, they are complicated and costly to manufacture. The new technology was developed through collaboration, including student exchanges, between the U.S. and KAUST researchers. Led by Qiaoqiang Gan and graduate student Lyu Zhou from The State University of New York at Buffalo, Jian-Wei Liang and colleagues from Boon Ooi’s Photonics Laboratory at KAUST, working with researchers from the University of Wisconsin, have developed a passive cooling technology made from a polydimethylsiloxane (PDMS)/aluminum film structure. “PDMS exhibits very high absorption in the Earth’s ‘atmospheric window’ range and low absorption in the solar visible wavelength range,” explains Liang. “These properties make it an ideal material for passive radiative cooling.” By exploiting the spectral overlap between this atmospheric window, corresponding to wavelengths between 8-13 microns and the range of thermal radiation emitted by buildings at typical ambient temperatures, the PDMS/

aluminum film can effectively cool buildings during daytime. To fabricate the film, the researchers used a blade-coating process to first coat the surface of an aluminum sheet with a layer of PDMS resin and then a metering blade to control its thickness, heating the structure in an oven at around 60 degrees Celsius for two hours to complete the process. “Although the PDMS has low absorption in the solar wavelength range, we found that its radiative cooling ability was significantly impacted by the surrounding environment when tested outdoors, especially in crowded urban settings,” says Gan. To address this, the team developed a spectral-selective shelter that directs the thermal radiation toward the sky and achieved a daytime temperature

reduction of up to 6.5 degrees Celsius in the outside environment. The PDMS/aluminum film provides a low-cost and greener solution to cooling buildings in urban environments and can also be manufactured on a large scale, contributing to the potential commercialization of radiative cooling technologies. “We are now working on the optical structure of the film to enhance its radiative cooling, as well as its application in vapor condensation and water cooling,” says Liang. Zhou, L., Song, H., Liang, J., Singer, M., Zhou, M., Stegenburgs, E., Zhang, N., Xu, C., Ng, T., Yu, Z. & Ooi, B. A polydimethylsiloxane-coated metal structure for all-day radiative cooling. Nature Sustainability 2, 718-724 (2019).

Jian-Wei Liang (left) and Lyu Zhou discuss the polymer film they manufactured.

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With the increase in the frequency of extreme weather events due to climate change, models to predict these disasters are becoming more important.

EXPANDING THE SCALE OF DANGEROUS WEATHER PREDICTION A more accurate and efficient method of capturing the

local factors that lead to extreme rainfall enables better flood prediction across larger regions. A statistical model that better characterizes the changing nature of extreme weather over larger areas could help climate experts plan for weather-related disasters. An increase in the severity of extreme weather events around the world, such as droughts and floods, is creating a need for information that will help us better plan for these extreme events. Although vast volumes of weather data are recorded every day across the globe, extracting crucial information on extreme events puts huge demands on computing power and is limited to analysis across only a few locations. Raphaël Huser and his former postdoc Daniela Castro-Camilo developed a computationally efficient statistical model to address these constraints. “One of the main challenges in extreme weather statistics is to describe

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“A s ev e n t s become more ex t r e m e, t h e data also tend to become less r e l a t e d .”

of locations at once and are not flexible enough to capture all the different dynamics we see in precipitation data.” To accurately predict the frequency and magnitude of an extreme weather event across an area, Castro-Camilo and Huser focused on the dependence structure, which describes how strongly, and in what way, the data at several locations are related to one another. “As events become more extreme, the data also tend to become less related,” says Castro-Camilo. “This behavior is well recognized in climatological data, but classical extreme-value models are not able to describe this characteristic. Our model can do this.” Castro-Camilo and Huser’s model allows the dependence structure to be estimated from each measurement station and then efficiently interpolated across stations over a fine spatial grid using a highly parallelized computational approach. “The main challenges in this study were in fact computational,” says Castro-Camilo. “Fortunately, we had access to KAUST’s Shaheen II supercomputer, which allowed us to obtain results in a few days rather than the months we might have had to wait if using a standard computer.” Using their new approach, the researchers looked for extreme events in precipitation data across the entire contiguous United States—a total of 1,218 weather stations, an unprecedented scale for such an analysis. They found that the dynamics that govern extreme precipitation events differ strongly across regions, and they quite clearly identified specific areas where dangerous levels of precipitation occurred simultaneously and with greater frequency.. “Our approach can also be used with other types of climatological data because it has been developed specifically to deal with high-dimensional problems involving many measurement stations,” says Castro-Camilo. Castro-Camilo, D. & Huser, R. Local

the relationship between extreme observations, such as rainfall changes across multiple locations,” explains CastroCamilo. “Current models and methods can deal with only a limited number

likelihood estimation of complex tail dependence structures, applied to U.S. precipitation extremes. Journal of the American Statistical Association 5 (2019).

NATIONAL GUARD / ALAMY STOCK PHOTO

CLEAN ENVIRONMENT

A LT E R N AT I V E F U E L S

BUILDING APPROACH FOR OPTOELECTRONICS STACKS UP A precise method for stacking semiconductor thin films enhances optoelectronic device performance using quantum effects.

created perovskite multiple quantum wells using a simple technique known as thermal evaporation. They started with powders of their chosen perovskite well material, CsPbBr3, and a barrier material, TPBi. These powders evaporated when heated in a vacuum chamber, and the vapor particles traveled to a substrate where they formed a film. The team alternated between heating the TPBi and the CsPbBr3 to make their quantum wells. Key to their success was calibration of the deposition rate. The team optimized the evaporation rates of their CsPbBr3 and TPBi powders at 0.015 and 0.020 nanometers per second, respectively. Unlike most epitaxial technologies, thermal evaporators are simple and widely available. Moreover, epitaxial methods need a substrate with a similar atomic lattice spacing to that of the deposited layer. The evaporation method, however, is applicable to any substrate; Lee and the team used simple glass because of the defect tolerance of perovskite materials. “I think this is just the beginning,” says Lee. “The study points in one unexplored direction in perovskite research, and we expect further exciting perovskite devices based on this work in the near future.”

A method to nanoengineer an emerging family of semiconductors known as perovskites could reduce the cost of highperformance optoelectronic devices. The properties of a semiconductor can be controlled by nanoscale engineering using technologies that slowly deposit atoms on a substrate. These methods are expensive and limited to conventional semiconductor materials, motivating scientists to search for new methods. Quantum wells are semiconductor films of just a few nanometers, sandwiched between two thicker layers of a difLee, K. J, Turedi, B., Sinatra, L., Zhumekenov, A. A. Maity, P. ferent semiconducting material. An energy barrier between Dursun, I., Naphade, R., Merdad, N., Alsalloum, A., Oh, S., Wehbe, the two materials blocks the electrical charge carriers from N., Hedhill, M., Kang, C.H., Subedi, R.C., Cho, N., Kim, J.S., Ooi, leaving the well layer, effectively limiting their motion to two B., Mohammed, O.F. & Bakr, O.M. Perovskite-based artificial dimensions. This radically alters the properties of the well multiple quantum wells. Nano Letters 6, 3535-3542 (2019). materials, making them more optically active, for example. This effect can be amplified further by combining multiple quantum wells into a single stack. Epitaxial methods—depositing crystalline film on a crystalline substrate—are used to construct such stacks from gallium arsenide or gallium nitride by expensive processes with specialized equipment. But another more practical approach is needed if this multiple quantum well architecture is to be used in perovskite devices. “Metal halide perovskites have excellent energy conversion efficiency for light harvesting and photoluminescence,” says postdoc Kwang Jae Lee from Osman Bakr’s lab in the KAUST Catalyst Center. Quantum wells could improve this efficiency still further. Working with colleagues from across KAUST and in collaboration with researchers A bulk perovskite single crystal becomes multiple quantum wells on a glass substrate using the thermalfrom Korea, Bakr, Lee and team evaporation technique. K AUST DISCOVERY

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A LT E R N AT I V E F U E L S

the cascade of chemical reactions involved in combustion processes. The hot, sometimes high-pressure, yet smooth conditions behind reflected shockwaves are the ideal environment for studying the chemical complexities of combustion. Aamir Farooq, from KAUST’s Clean Combustion Research Center, and his team have used a shock tube coupled with laser diagnostics to study the rapid cascade of chemical reactions set in motion when fuel combusts. Their results can help in the design of cleaner, more efficient engines and fuels. The insights gained could also be used to study reactions in the air that generate or remove pollutants, or even to study the atmospheric conditions of distant planets. “Shock tubes are ideal chemical reactors because of the nearly homogeneous zerodimensional conditions behind reflected shockwaves,” Farooq says. The team shines lasers through the shock tube to monitor the chemistry taking place. “Laser diagnostics enable us to make in situ measurements of chemical species being consumed and formed during a chemical reaction,” Farooq adds. “We can track highly reactive free radicals, which play a key role in combustion kinetics.” Two recent papers illustrate the breadth of information that can be acquired. Farooq and his team investigated the combustion chemistry of cyclic ketones, which can be made from plant waste and have excellent combustion behavior1. “Biomassderived cyclic ketones attract interest due to their good antiknock property and their effectiveness in reducing harmful emissions,” says Dapeng Liu, a Ph.D. student in Farooq’s team. Reactions with hydroxyl radicals are among the most important reactions initiating the

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combustion of cyclic ketones, but these had never been experimentally measured before at high temperatures. “Compared with our measurements, researchers had overestimated the reactivity of cyclic ketone and hydroxyl reactions at high temperatures, but underestimated it for room temperature conditions,” says Liu. This new data will improve models used to design fuels incorporating cyclic ketones. The team also studied hydroxyl reactions with diolefins, common molecules featuring two carbon-carbon double bonds2. This interaction is significant for fuel combustion, but also for atmospheric chemistry. “Isoprene, a well-known diolefin, is produced by animals and plants and can be found at high concentration in forest areas,” says Fethi Khaled, who recently completed his Ph.D. with Farooq and is now undertaking a postdoc at postdoctorate at Université d’Orléans. “Our work showed the rich chemistry of hydroxyl radicals and diolefins,”

Khaled says. The team revealed a clear shift in reaction pathways such that rather than hydroxyl radicals being added to diolefins, hydroxyl radical are plucked from diolefins as temperatures increase up to combustion conditions. The results add to the growing database of reaction rate coefficients the team has provided, which is used widely by chemical kinetic modelers and theoreticians to validate their calculations, says Farooq. “In future, we are going to focus on radical plus radical reactions, which are much more challenging to study but play a critical role in many chemical environments,” he says. “We are designing new laser diagnostics to detect a wide array of molecules, so we can paint a complete picture of complex chemical reactions,” Farooq adds. “Finally, we are extending our methodologies to study reactions relevant to atmospheric chemistry and interstellar planets.” 1. Khaled, F., Giri, B. R., Liu, D., Assaf, E., Fittschen, C.& Farooq, A. Insights into the reactions of hydroxyl radical with diolefins from atmospheric to combustion environments. Journal of Physical Chemistry A 123, 2261-2271 (2019). 2. Liu, D., Giri, B. R. & Farooq, A. Cyclic ketones as future fuels: Reactivity with OH radicals. Journal of Physical Chemistry A 123,

2019 KAUST; HENO HWANG

CHEMICAL ENLIGHTENMENT BEHIND REFLECTED SHOCKWAVES Studying the wake of reflected shockwaves reveals

4325-4322 (2019).

The insights gained by studying chemical reactions in a shock tube could lead to cleaner fuels and cleaner air.

A LT E R N AT I V E F U E L S the active layer, charge-carrier mobility and charge recombination rate, on the performance of nonfullerene organic solar cells. Postdoctoral fellow Yuliar Firdaus explains that the simulations explicitly treat the effect of these parameters. Therefore, the calculated cell efficiency limit is similar to the efficiency that nonfullerenebased cells can realistically achieve with continued material improvement.

“N o n f u l l e r e n e based cells will soon reach these calcuYuliar Firdaus and colleagues have developed a computational approach to predict efficiency limits and propose design rules for nonfullerene organic solar cells.

BENCHMARKS TO BETTER CATCH THE SUN Simulations unveil efficiency targets and design rules to maximize the conversion of light into electricity using organic solar cells. Organic solar cells could soon rival traditional silicon-based photovoltaic technologies in terms of conversion efficiency. A team from the KAUST Solar Center has developed a computational approach that provides practical performance targets and useful rules to help design and develop material systems for optimal organic solar cells. Most solar panels rely on inorganic semiconductors to harvest and convert sunlight into electricity. Organic photovoltaic materials, however, have emerged as lightweight, inexpensive alternatives. These materials are easy to tune and process at large scales, which makes them appealing for industrial production and commercialization. State-of-the-art organic solar cells rely on bulk heterojunctions, which combine light-responsive electron donor and acceptor materials to form an active layer. Exposure to sunlight creates an excited state that

generates pairs of electrons and positively charged holes, which are responsible for electric current. These charge carriers need to be held apart, an action that relies on the electron donor and acceptor materials. Fullerene-based acceptor materials have yielded organic solar cells with unparalleled conversion efficiencies for almost two decades. However, these materials have several drawbacks, such as high voltage losses and poor absorption of the solar spectrum, which have restricted efficiencies to 11 percent. Meanwhile, nonfullerene alternatives have recently outperformed all existing fullerene-based cells, but a lack of understanding of the elements that control the conversion efficiency of these cells has limited further enhancement in cell performance. Thomas Anthopoulos and coworkers used computer simulations to assess the influence of several key parameters, including the absorption and thickness of

lated efficiency l i m i t s .” The researchers found that nonfullerene-based cells could realize efficiencies exceeding 18 percent, even with the readily achievable charge mobility in existing material systems. Efficiencies could even surpass 20 percent with high and balanced electron and hole mobilities associated with low recombination rate constants. “I am confident that the nonfullerene-based cells will soon reach these calculated efficiency limits,” Firdaus says. “We are presently working on different fronts, such as developing new interfacial layers and dopant formulations, while maintaining the same primary goal: pushing the efficiency of organic solar cells closer to the practical limits identified in our study,” Firdaus says. Firdaus, Y., Le Corre, V.M., Khan, J.I., Kan, Z., Laquai, F., Beaujuge, P.M. & Anthopoulos, T.D. Key parameters requirements for non-fullerenebased organic solar cells with power conversion efficiency >20%. Advanced Science 6 (2019).

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FLEXIBLE THINKING ON SILICON SOLAR CELLS Combining silicon with a highly elastic polymer backing produces solar cells that have record-breaking stretchability and high efficiency. Crystalline silicon solar panels could be just as effective when incorporated into stretchy wearable electronics or flexible robot skin as they are when used as rigid rooftop panels. KAUST researchers have devised a way to turn rigid silicon into solar cells that can be stretched by a record-breaking 95 percent, yet retain high solar energy capture efficiency of 19 percent Although many new solar materials are being investigated, silicon remains by far the photovoltaic (PV) industry’s favorite. “Monocrystalline silicon remains the material of choice in the PV industry due to its low cost, non-toxicity, excellent

reliability, good efficiency and maturity of the manufacturing process,” says Nazek El-Atab, a postdoctoral researcher in the labs of Muhammad Mustafa Hussain, who led the research. One drawback of silicon for certain applications is its rigidity, unlike some thin film solar cells. However, these flexible cells either consist of low-cost, low-efficiency organic materials, or more efficient but very expensive inorganic materials. Hussain and his team have now taken a significant step toward overcoming this limitation by

developing low-cost, high-efficiency siliconbased stretchy solar cells. The key step was to take a commercially available rigid silicon panel and coat the back of the panel with a highly stretchable, inexpensive, biocompatible elastomer, called ecoflex. The team then used a laser to cut the rigid cell into multiple silicon islands, which were held together by the elastomer backing. Each silicon island remained electrically connected to its neighbors via interdigitated back contacts that ran the length of the flexible solar cell. The team initially made rectangle-shaped silicon islands, which could be stretched to around 54 percent, Hussain says. “Beyond this value, the strain of stretching led to diagonal cracks within the brittle silicon islands,” he says. The team tried different designs to push the stretchability further, mindful that each slice of silicon they removed reduced the area available for light capture. The team tried a diamond pattern, before settling on triangles. “Using the triangular pattern, we achieve world-record stretchability and efficiency,” Hussain says. The team plans to incorporate the stretchy silicon solar material to power a multisensory artificial skin developed by Hussain’s lab. Making solar panels that stretch with even greater flexibility is also a target. “The demonstrated solar cells can be mainly stretched in one direction, parallel to the interdigitated back contacts grid,” Hussain says. “We are working to improve the multidirectional stretching capability.” El-Atab, N., Qaiser, N., Bahabry, R. & Hussain, M.M. Corrugation enabled asymmetrically ultrastretchable (95%) monocrystalline silicon solar cells with high efficiency (19%). Advanced Energy Letters (2019).

NAZEK EL-ATAB POSTDOC In Muhammad Mustafa Hussain’s group, Nazek focuses on the design and fabrication of futuristic electronics.

Highly flexible solar panels can be used effectively in moving robots.

2019 KAUST; HENO HWANG

A LT E R N AT I V E F U E L S

This sequence captures the fabrication process of a perovskite thin film from precursor solution to solid film via the spin-coating deposition process.

TINY TWEAKS FOR BIG WINS IN SOLAR CELLS Changes in composition are shown to affect light-harvesting layer crystallization and perovskite solar cell efficiency. Solar cells that rely on perovskites to harvest sunlight are bound to gain in energy conversion efficiency thanks to an atomiclevel understanding of the structure-property relationship of these photovoltaic materials. Researchers from the KAUST Solar Center monitored the impact of compositional changes on the structural organization and photovoltaic properties of perovskite thin films in situ1, 2. Hybrid perovskites have emerged as key components in low-cost, high-efficiency solar cells because they are cheaper and easier to process than traditional silicon-based solar cell materials. In addition, they exhibit unique optoelectronic characteristics, including high light absorption and a defect tolerance, that lead to solar cells with maximum power-conversion efficiencies of 24 to 28 percent when used alone or in tandem combination with silicon. They also outperform single-junction silicon solar cells. Solar cell performance and stability depend on the morphology of the thin films, especially their ability to crystallize in the so-called photoactive α-phase.

Perovskites containing lead tend to combine various halides, such as the anionic forms of bromine and iodine, with mixtures of methylammonium, formamidinium, cesium and other cations. These have led to record conversion efficiencies and thermal stabilities compared with their single-halide, single-cation analogs. However, these mixed-halide, mixed-cation perovskite films have been characterized only through ex situ postdeposition techniques. This limits the understanding of the mechanisms that govern their growth from their sol-gel precursor to their solid state and stalls attempts to improve device performance and stability. Now, Stefaan De Wolf, his postdoc Kai Wang and coworkers have investigated the impact of cations, halides and antisolvent dripping on mixed-halide, mixed-cation perovskite films. The team tracked the films’ structural evolution during the spincoating deposition process using an in situ X-ray scattering technique. The X-ray technique probed the films at the atomic scale

from their sol-gel precursor to the solid state and provided information about the formation of crystalline intermediates during the solidification. The researchers also incorporated the films into solar cells and evaluated the performance and stability of the resulting devices. “Our study provides critical insights into the crystallization of the multicomponent systems toward high-performance perovskite solar cells,” Wang says. Changes in the compositions of the halide and cation dramatically affected the solidification of the perovskite precursors during spin coating and the subsequent formation of the desired α-phase upon antisolvent addition. The period needed to generate highquality films by antisolvent addition ended when the sol-gel structure collapsed to produce crystalline by-products depending on the precursor mixture. Consequently, tuning the halide-cation mixture could delay this collapse, widening the antisolvent dripping window from a few seconds to several minutes. As well, simultaneously incorporating cesium and rubidium cations in the perovskite synergistically stimulated the formation of the α-phase. The length of this window showed little effect on resulting solar cell performance as long as the antisolvent was added within this period. These findings suggest new directions for the development of perovskite formulations that can further stabilize the sol-gel state and promote its conversion to the desirable perovskite phase. “This is critical in achieving better-performing, reproducible, cost-efficient and scalable manufacturing of perovskite solar cells,” De Wolf says. The team is working on transferring this knowledge to other deposition technologies to progress toward market-ready perovskite solar cells. 1. Dang, H. X., Wang, K., Ghasemi, M., Tang, M.-C., De Bastiani, M., Aydin, E., Dauzon, E., Barrit, D., Peng, J., Smilgies, D.-M & De Wolf, S. Multi-cation synergy suppresses phase segregation in mixed-halide perovskites. Joule 7, 1746-1764 (2019). 2. Wang, K., Tang, M.-C., Dang, H. X., Munir, R., Barrit, D. De Bastiani, M., Aydin, E., Smilgies, D.-M.,De Wolf, S. & Amassian, A. Kinetic stabilization of the sol-gel state in perovskites enables facile processing of high-efficiency solar cells. Advanced Materials (2019).

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R EE XD P LSOERAI N G T H E R E D S E A

Macroalgae, like this seaweed, sequester carbon and can sink to the depths of the ocean.

SEAWEED SINKS DEEP, TAKING CARBON WITH IT Macroalgae is shown to be a major global contributor to carbon sequestration.

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Seaweed may be a quiet achiever when it comes to mitigation of greenhouse gases, with it now shown to travel far and deep beyond coastal areas and thus to play a key role in sequestering carbon from the atmosphere. Seaweed, or macroalgae, forms the most extensive and productive vegetated coastal habitats. It colonizes all latitudes and is efficient at capturing atmospheric CO2 and converting it into plant material. An international research team has reported that a diverse range of macroalgae species drifts as much as 5,000 kilometers beyond coastal areas. Around 70 percent of this seaweed, and

not remain in the same place but drift with currents and tides. Little is known about their fate once they have floated away from the coast. As a result, there have been no detailed assessments of their role in carbon sequestration in coastal habitats, particularly in the sediments of seagrass and mangrove. The international team led by Carlos Duarte, including KAUST colleagues at the Red Sea Research Center and the Computational Bioscience Research

Carbon sequestered in seaweed can sink to ocean depths below

1,000

“H u g e i m p l i c a tions for how the global carb o n d i ox i d e b u d g e t i s c a lc u l a t e d .”

therefore carbon, will sink to ocean depths below 1,000 meters, meaning that this captured carbon is unlikely to return to the atmosphere. “This finding has huge implications for how the global carbon dioxide budget is calculated,” says Ph.D. student Alejandra Ortega, the first author of the study. “It indicates that macroalgae are important for carbon sequestration and should be included in assessments of carbon accumulated in the ocean, known as blue carbon.” Macroalgae are ignored in current assessments of blue carbon, mainly because these rootless marine plants do

meters

Center (CBRC), has identified DNA sequences of macroalgae in hundreds of metagenomes generated by the global ocean expeditions Tara Oceans and Malaspina, the latter led by Duarte. The expeditions surveyed the global ocean to a depth of 4,000 meters and sequenced the particulate material collected in the water sample to create a global DNA resource. The marine scientists searched for macroalgae in these global ocean metagenomes using Dragon Metagenomic Analysis Platform (DMAP). Developed by CBRC bioinformaticians, DMAP uses KAUST’s supercomputer to annotate and compare metagenomic data sets. For the very first time, the team was able to provide semiquantitative evidence of the presence of macroalgae beyond the shoreline. “Work is still needed to be able to translate a specific amount of DNA into a specific amount of organic carbon in a specific taxon, but finding macroalgal DNA is the first step,” says Ortega. Ortega, A., Geraldi, N., Alam, I., Kamau, A., Acinas, S., Logares, R., Gasol, J., Massana, R., Krause-Jensen, D. & Duarte, C. Macroalgae are important contributors to oceanic carbon export and sequestration. Nature Geoscience 12, 748–754 (2019).

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EXPLORING THE RED SEA

GIANT CLAMS TRAP MARINE PLASTICS Microplastics in the water column are ingested by clams and become attached to their shells. Giant clams take up a large fraction of marine microplastics,1 which could help explain the mystery of the plastic that is “missing” from the Red Sea. Researchers at the Red Sea Research Center have previously shown that the Red Sea has relatively low amounts of floating

Spring 2020

plastic debris in its surface waters,2 yet the reason for this has remained elusive. Now, they have assessed the role of giant clams as a potential sink for marine plastics, with some surprising results. Twenty-four giant clams collected from the Red Sea were put into aquariums with

plastic beads from 53 to 500 micrometers in size—the size range reported as missing from the Red Sea in a 2017 survey. By measuring the change in microplastic concentration after 12 days and counting the beads in the clams’ digestive system and on their shells, the team assessed how much plastic the clams captured. Their analysis revealed that the clams ingest beads, with each consuming about 100 beads during the experiment. While larger clams tended to consume larger beads, smaller clams did not have a size preference, and the amount consumed did not depend on bead concentration. To the team’s surprise, this active uptake

EXPLORING THE RED SEA

Silvia Arossa and colleagues found that tiny pieces of plastic attach to the shells of giant clams living in the Red Sea.

“T h e c l a m s ingest beads, with each consuming about 100 beads during t h e ex p e r i m e n t .”

to the surface of marine organisms. “Most people probably know that animals in the sea eat marine plastic, but they probably don’t realize that it can also accumulate on the surface of animals and affect not only the organism itself but also the ecosystem in general,” says Arossa. Microplastics accumulate up the food chain, eventually finding their way into humans, and they also readily absorb contaminants. While the removal of microplastics by clams may seem to benefit the ecosystem, Arossa argues that the quantity removed is tiny compared to the amount of plastic pollution in the oceans. In other words, the harm done to the clams probably outweighs any potential benefits of plastic removal from the ecosystem. “We should find alternative ways to fix this problem.” she says. Such solutions need to include preventing plastic waste from polluting marine ecosystems in the first place. This study not only offers a partial explanation for the low density of microplastics in the water column in the Red Sea, but it also demonstrates the importance of studying the 3D structure of organisms and ecosystems to understand the fate of microplastics in marine ecosystems. 1. Arossa, S., Martin C., Rossbach, S. & Duarte, C.M. Microplastic removal by Red Sea giant clam (Tridacna maxima). Environmental Pollution 252, 1257-1266 (2019). 2. Martí, E., Martin, C., Cózar, A. & Duarte, C.M. Low abundance of plastic fragments in the surface waters of the Red Sea. Frontiers in Marine Science 4 (2017).

accounted for only a small fraction of the plastic the clams captured. “At the beginning, we were focused on ingestion, but then we realized that most of the plastic was attached to the surface of the shells,” explains Ph.D. student Silvia Arossa, the study’s lead author. Passive accumulation on shells captured 30 to 100 times as many beads as ingestion, removing about 66 percent of the microplastic from the water column. Clam size had no effect on the number or size of the attached beads but more beads were captured as the concentration increased. This is one of the first studies to investigate how much plastic becomes attached K AUST DISCOVERY

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RED SEA

Aiptasia is often used as a model for reef-building corals.

CORALS TAKE CONTROL OF NITROGEN RECYCLING Corals use sugar from their symbiotic algal partners to control them by recycling nitrogen from their own ammonium waste. Corals are shown to recycle their own ammonium waste using a surprising source of glucose—a finding that reveals more than was previously known about the relationship between corals and their symbiotic algae. Symbiosis between corals and algae provides the backbone for building coral reefs, particularly in nutrient-poor waters, like the Red Sea. Algae

Spring 2020

and corals cooperate to share nutrient resources, but the precise metabolic interactions at play are still unclear. Now, KAUST researchers have shown that the coral host uses organic carbon—in glucose sourced from its symbiotic algae—to recycle its own ammonium waste. Previous research had suggested that the algae alone may be responsible for ammonium (nitrogen)

recycling. The team believes that, by controlling this nitrogen recycling mechanism, the coral host can in turn control algal growth by restricting or enabling nitrogen flow. “Molecular research on coral-algae symbiosis is relatively young. The first genetic sequencing study focusing on the coral model anemone Aiptasia was published in 2014,” says Guoxin Cui at the

Red Sea Research Center, who worked on the project under the supervision of Manuel Aranda. “To explore the molecular mechanisms underlying Aiptasia’s symbiotic relationship with the algae Symbiodiniaceae, we first integrated all published RNA-sequencing data on this relationship and conducted a meta-analysis.” Meta-analysis is a statistical method originally developed for medical research, to calculate the precise effects of a specific medicine on patients with a specific disease by combining results from multiple trials. “In our case, each gene could be seen as an individual ‘medicine,’ and we can calculate the effect of each gene on symbiosis by monitoring its expression changes across many experiments,” says Cui.

EXPLORING THE RED SEA

“O u r r e s u l t s s h o w that competition for nitrogen is a ke y m e c h a n i s m

1,000+

Students from over 75 countries

w i t h i n c o ra l - a l g a e s y m b i o s i s .” “Because we use large datasets compiled from multiple studies, we can be pretty confident of the effect size we calculate for each gene. By focusing on those genes that are definitely associated with symbiosis, we can eliminate noise from unwanted parameters.” Once the team had identified a set of high-confidence genes, they set up a metabolomics experiment, with the help of their colleagues in the Core Labs, using symbiotic and nonsymbiotic (or bleached) Aiptasia. They placed the anemones in water and added bicarbonate containing labeled carbon-13 (13C) isotopes. The symbiotic algae absorbed the bicarbonate during photosynthesis, transferring the 13C signal to the host’s metabolites. The team could then follow the carbon isotope through the metabolic pathways of the anemones and determine which were enriched with 13C. “Our results show that competition for nitrogen is a key mechanism within coral-algae symbiosis,” says Cui. “These insights will help us understand what goes wrong when the relationship is placed under stress, for example, because of shifting climates.” Cui, G., Liew, Y.J., Li, Y., Kharbatia, N., Zahran, N.I., Emwas, A.-H. Eguilus, V.M. & Aranda, M. Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia. PLOS Genetics 15 (2019).

Join an international community dedicated to science & technology innovation. BLEACHED UNBLEACHED The gray animal (left) is in an aposymbiotic (bleached) state, while the red animal is the symbiotic state.

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Core Labs

IN THE GROWTH CHAMBER FACILITY, RESEARCHERS EVALUATE SEEDLING HEALTH AS AN INDICATION OF SUCCESS IN THE LAB. From here, scientists move the plants forward to the greenhouse or they may head back to the lab.

discovery.kaust.edu.sa 22

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2019 CHARLOTTE YOUNG

EXPLORING THE RED SEA

Unusually high sea temperatures can cause healthy corals (left) to become bleached.

CHANGING HOW WE PREDICT CORAL BLEACHING

A remote sensing algorithm offers better predictions of Red Sea coral bleaching and can be fine-tuned for use in other tropical marine ecosystems. Coral bleaching events may occur more frequently in the Red Sea than previously thought, according to an algorithm developed by KAUST researchers. Their findings also indicate that the northern part of the Red Sea might not remain a thermal refuge for coral ecosystems for long. Ocean modeling expert Ibrahim Hoteit and colleagues used more than 30 years of satellite data on Red Sea surface temperatures to develop an algorithm that successfully isolated every extreme warming event that led to documented coral bleaching in the Red Sea. Their approach suggests that coral bleaching in the Red Sea may be greatly underestimated. When exposed to unusually high sea surface temperatures for prolonged periods, corals expel the marine algae that live within them. Because these algae serve as the corals’ main energy source, in their absence, coral colonies turn a deadly looking white, a phenomenon known as

coral bleaching. If the adverse conditions continue, it becomes difficult for the corals to regain the algae and so they tend to die, in turn affecting the coral reef ecosystem that depends on them for survival. Red Sea surface temperatures are among the warmest in the world, and its corals are thought to be among the most heat tolerant. But Red Sea corals are poorly monitored, and therefore little is known about the true extent of their damage due to rising temperatures. “It is important to detect bleachingprone regions in the Red Sea because this allows us to optimize the sustainable management of the coastline by identifying the areas most in need of mitigation plans to reduce the stress on corals,” says Ph.D. student Lily Genevier. The team calculated marine heatwaves by pooling sea surface temperatures around each day of the year to find that bleaching occurred during summer marine heatwaves where sea surface

temperatures remained in the top five percent for at least a week. “Because the marine heatwave threshold is based on a percentile, it follows seasonality, meaning it can detect extreme anomalous heating during cooler summer periods,” Genevier explains. They also found that all documented bleaching events happened during marine heatwaves with a mean sea surface temperature of 30 degrees Celsius or higher. The findings suggest that Red Sea coral bleaching may have been greatly underestimated. They also indicate an emerging pattern of extreme warming events in the northern region, which was previously thought to act as a thermal refuge for corals. “Because this study was able to detect bleaching-prone areas using only the few known bleaching events in the Red Sea, we think it should be applied to other data-poor regions,” says Genevier. The team is now working on implementing its methodology on a global scale by tuning marine heatwaves to bleaching conditions in other tropical marine ecosystems. They plan to upload their results onto the interactive online Red Sea Atlas being developed at KAUST. Genevier, L.G.C., Jamil, T., Raitsos, D.E., Krokos, G. & Hoteit, I. Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea. Global Change Biology 25, 2338-2351 (2019).

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NOV EL M ATERI A L S

LIGANDS STABILIZE NANOCLUSTERS TO MAKE THEM BRIGHTER Large cylindrical ligands increase stability and enhance light emission of silver nanoclusters.

various functional groups, which allows them to hold electron-poor and neutral compounds in their cavity. This is expected to widen the range of potential guest molecules and, consequently, the ability to tailor the properties of the nanoclusters. The pillararene-functionalized nanoclusters remained stable for four months when stored in the dark and up to seven days when exposed to daylight. Their photoluminescence rose 30 times when a neutral amine was used as a guest molecule. Adding the cationic surfactant cetrimonium bromide induced a 2,000-fold increase in photoluminescence that was visible to the naked eye, and also outperformed other atomically precise nanoclusters. The researchers demonstrated that stronger binding between guest molecules and nanoclusters led to a more pronounced increase in photoluminescence. This suggests that the dramatic increase in emission results from hostguest interactions. This system could have useful biological applications, especially in noninvasive deep-tissue imaging,” says Khalil. This will help diagnose diseases, such as skin cancer and brain anomalies.

Metal nanoclusters that bear tunable surface ligands could help develop next-generation imaging and photocatalytic approaches, suggest KAUST researchers. Metal nanoclusters, usually less than two nanometers in size, exhibit unique physical and chemical characteristics that are useful for a multitude of applications ranging from catalysis and sensing to imaging and drug delivery. These properties hinge on Muhammed, M., Cruz, L. K., Emwas, A.-H., El-Zohry, A., Moosa, the size and stability of the nanoclusters. Several ligands have B., Muhammed, O.F. & Khashab, N.M. Pillar[5]arene stabilized proven to be effective for stabilizing the nanoclusters and tuning silver nanoclusters: extraordinary stability and luminescence their properties according to specific uses. However, these sizeenhancement induced by host-guest interactions. Angewante dependent properties remain difficult to harness. Chemie International Edition 58, 15665-15670 (2019). Silver nanoclusters tend to have low stability. Although some of these nanoclusters remain stable over a few days, most disintegrate within minutes, explains Ph.D. student Laila Khalil. This LAILA KHALIL demise highlights the need for stabilizing ligands that can also PH.D. STUDENT In Niveen Khashab’s research group, Laila is improve the optical properties of these nanoclusters. focused on the design of porous organic and Now, a team led by Niveen Khashab with coworkers from the metallorganic materials, merging supramolecular University’s Core Labs have devised a way to increase stability. and macrocyclic chemistry, toward the They developed sulfur-based ligands with a large cyclic funcdevelopment of new, highly guest-responsive materials. tional group called pillararene. These ligands can simultaneously stabilize silver nanoclusters and feature a cylindrical cavity that can accommodate small molecules, or guests, and selectively bind to these guests through noncovalent interactions. “We create and synthesize systems that mimic natural designs,” says Khalil to explain why the team decided to produce a macrocyclic thiol ligand. Unlike typical macrocycle-based ligands, such as hydrophobic and cone-shaped calixarenes, pillararenes are electron-rich cylindrical structures that Noncovalent interactions between pillararene-based ligands and cationic cetrimonium bromide generate selfcan be readily modified using assembled structures that are more stable and better lit.

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NOV EL M ATERI A L S quarterpolymers—leads to even greater incompatibility. Hadjichristidis and his team have developed a trick, called catalyst switching, to help overcome the incompatibility problem. Most organic catalysts that are used for a polymer-forming reaction, called ring-opening polymerization, are either acids or bases. By adding one type of

“T h i s s t ra t e g y s av e s t i m e a n d a l s o av o i d s t h e risk of any contamination of the Hadjichristidis and his team found that using catalyst switching saves time and avoids the risk of any contamination of the polymer.

CATALYST SWITCHING MEANS FOUR BECOME ONE

Catalyst switching strategy is the key step in the production of a four-component crystalline tetrablock quarterpolymer. By juggling four different chemical reactions in a single flask, researchers have combined four polymers to form a single multicrystalline substance. Materials that seamlessly combine multiple polymers potentially merge the best aspects of each material. The versatile new approach for creating these “multicrystalline multiblock polymers,” developed by Nikos Hadjichristidis from the KAUST Catalysis Center and his team, in collaboration with Yves Gnanou, could lead to a whole new family of advanced polymer materials. Polymers are long-chain molecules made by connecting together small molecule “monomeric units,” like a string of identical beads on a necklace. Recently, researchers have developed ways to make “double-crystalline” copolymers

in which one part of the chain is made from one kind of monomer and the other part is made from another. “Doublecrystalline block copolymers have myriad applications, such as for energy storage, tissue engineering, and drug delivery,” says Viko Ladelta, a member of Hadjichristidis’s team. Adding a greater number of different polymer sections has the potential to produce materials with even more advanced properties. “But the synthetic procedures are very demanding,” Ladelta explains. “It was difficult to perform even the synthesis of double-crystalline block copolymers due to the incompatibility of the monomers and catalysts.” Making materials that incorporate four different monomers in four chemically different blocks—tetra-crystalline tetrablock

p o l y m e r.” monomer to the polymer chain under basic conditions, then adjusting the pH and using a second catalyst to add the next monomer, it is possible to create multiblock polymers in a single reaction pot. “This strategy saves time and also avoids the risk of any contamination of the polymer,” Ladelta says. Hadjichristidis’s group has previously used catalyst switching between organic catalysts to create double-crystalline and triple-crystalline polymers. Now, for the first time, the team has shown that it is possible to adjust the pH and then switch from an organic to a metal catalyst to make a tetracrystalline tetrablock quarterpolymer. “Our plan is to expand the scope of the catalyst switching strategy to other types of polymerization,” Ladelta says. “We will synthesize more complex multicrystalline polymers and collaborate with polymer physicists to understand the physical properties to guide us toward real-world applications.” Ladelta, V., Zapsas, G., Abou-hamad, E., Gnanou, Y. & Hadjichristidis, N. Tetracrystalline tetrablock quarterpolymers: Four different crystallites under the same roof. Angewandte Chemie International Edition 58, 16267-16274 (2019).

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Weiwei Li (left) and Atif Shamim inspect their transparent electronic devices.

BABY STEPS FOR TRANSPARENT ELECTRONICS

Stretchy, see-through silver nanowire sheets combine optical transparency with excellent electrical conductivity.

Spring 2020

A submicrometer-thin mesh of silver nanowires that is transparent to light, highly electrically conductive, flexible and stretchable, and simple to make has been developed by researchers at KAUST. The material could find use in flexible electronic displays, sensors, solar cells or even incubators for newborn babies. “The idea came to me when I was in the hospital with my son, who was in an incubator,” recalls Atif Shamim. “I worried about the exposure of the babies to all the electromagnetic radiation in the room,” he says. While opaque metals are well known for their electrical conductivity, serving as blocks to electromagnetic radiation, they are generally not transparent or stretchable. “We didn’t want to protect the incubators against the radiation by using metal because then we wouldn’t

NOV EL M ATERI A L S

A nanowire is a linear nanostructure with a diameter of

ONE BILLIONTH

of a meter (10-9) or less.

“We d i d n’ t wa n t t o p r o tect the incubators a g a i n s t t h e ra d i a t i o n by u s i n g m e t a l b e c a u s e t h e n w e w o u l d n’ t b e a b l e t o s e e t h e i n f a n t s .”

be able to see the infants,” he explains. There are printed films of metal nanowires, in which the conductive metal nanowires are so thin that light can pass between them. However, it has been challenging to directly create nanowire sheets that simultaneously have high conductivity, high transparency, flexibility and stretchability. “Now, we have found a solution to this problem,” explains Weiwei Li, a postdoctoral researcher in Shamim’s team. First, the team refined the method for making silver nanowires, adapting the previous protocol to make larger quantities of longer nanowires. The nanowires could be used directly in a new ink formulation that resulted in a uniform layer of silver when applied by screen printing onto a flexible substrate. Thanks to the length of the nanowires, the team could achieve high conductivity with a relatively sparse covering of nanowires that in turn increased the optical transparency. In a final manufacturing step, the team used laser sintering to weld together adjacent nanowires at points of contact: this increased the electrical conductivity further while also reducing the thickness of the silver layer and letting even more light pass through. The material maintained its electrical performance even after 1,000 stretch-release cycles and 1,000 bending cycles. The team tested their material’s performance by printing the conductive ink in patterns that enabled it to absorb predetermined wavelengths of electromagnetic radiation. “With the huge number of wireless devices, we are all exposed to electromagnetic radiation all the time,” Li says. “We designed special electromagnetic absorbers using our transparent ink, which can absorb more than 90 percent of the electromagnetic signals in a specific frequency band,” he explains. “We believe that this work will benefit the development of future flexible, transparent and stretchable conductive electronics at low cost and at large scale,” says Shamim. Li, W., Yang, S. & Shamim, A. Screen printing of silver nanowires: balancing conductivity with transparency while maintaining flexibility and stretchability. npj Flexible Electronics 3, 13 (2019).

K AUST DISCOVERY

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QUANTUM DESTABILIZATION OF A WATER SANDWICH When a thin layer of water is squeezed between two hydrophobic surfaces, the laws of classical physics break down.

Spring 2020

Measuring forces between hydrophobic surfaces at molecular resolution pinpoints the contribution of the quantum nature of water’s hydrogen atoms to the hydrophobic interaction.

atoms are replaced by a heavier hydrogen isotope called deuterium. “Our surface force measurements revealed that the attractive force was always approximately 10 percent higher in H2O than in D2O,” says Sreekiran Pillai, a Ph.D. student in Mishra’s lab. Collaborating with Tod Pascal at the University of California San Diego, the team came up with an explanation. The smaller an object, the less strictly it is governed by the laws of classical physics and the more it is subject to quantum effects. The tiny hydrogen atom is a quantum object—sometimes behaving like a particle, sometimes more like a wave. Deuterium, twice as heavy as hydrogen, is less subject to quantum effects. The consequence is that D2O is less destabilized than H2O

when squeezed between two hydrophobic surfaces and the hydrogen bonds between water molecules get broken. The discovery may have practical implications, Mishra says. “For example, these findings might aid the development of nanofluidic platforms for molecular separation.” “This is very impressive work that shows how quantum nuclear effects in water become substantial on the nanoscale,” explains Professor Mischa Bonn, director of the Max Planck Institute for Polymer Research. “The results illustrate that there is still much to learn about water at the fundamental level, yet with direct relevance to nanoscale-confined water in, for instance, nanopores used for water purification and desalination.” Shrestha, B.R., Pillai, S., Santana, A., Donaldson Jr, S.H., Pascal, T.A. & Mishra, H. Nuclear quantum effects in hydrophobic nanoconfinement. Journal of Physical Chemistry Letters 10, 55305535 (2019).

2019 KAUST; XAVIER PITA

From raindrops rolling off the waxy surface of a waterlily leaf to the efficiency of desalination membranes, interactions between water molecules and waterrepellent “hydrophobic” surfaces are all around us. The interplay becomes even more intriguing when a thin water layer becomes sandwiched between two hydrophobic surfaces, researchers have shown. In the early 1980s, researchers first noted an unexpected effect when two hydrophobic surfaces were slowly brought together in water. “At some point, the two surfaces would suddenly jump into contact—like two magnets being brought together,” says Himanshu Mishra from KAUST’s Water Desalination and Reuse Center. Mishra’s lab investigates water at all length scales, from reducing water consumption in agriculture to the properties of individual water molecules. Because researchers were unable to explain the phenomenon at the molecular level, in 2016, Mishra organized a conference on the subject. “We brought together leaders in the field— experimentalists and theorists—leading to intense debates on the understanding of hydrophobic surface forces,” he says. Part of the challenge was that the hydrophobic interaction is unique to water. “Gaining insights through other liquids or adding cosolvents to water is not feasible: the interaction is dramatically reduced or lost,” explains Buddha Shrestha, a postdoctoral researcher in Mishra’s lab. Inspired by the conference, Mishra came up with the idea of comparing ordinary water with “heavy water,” in which the hydrogen

NOV EL M ATERI A L S

MAGNETIC SKIN ENSURES THE FORCE IS WITH YOU

A magnetic skin that is safe and comfortable to wear could open the door to a wide range of wireless, remotely controlled applications. Who hasn’t unleashed their inner Jedi to use “the force” to open automatic doors at the shopping mall? A novel magnetic skin has been developed at KAUST that can remotely control switches and keyboards with the wave of a hand or the blink of an eye. The artificial skin is wearable, flexible, lightweight and magnetized, making it useful in a variety of applications without the need for a wired connection to other devices. “Artificial electronic skins typically require a power supply and data storage or a communication network. This involves batteries, wires, electronic chips and antennas and makes the skins inconvenient to wear,” says electrical engineer Jurgen Kosel, who led the project. “Our magnetic skin does not require any of this. To the best of our knowledge, it is the first of its kind.” The skin is made using an ultraflexible, biocompatible polymer matrix filled with magnetized microparticles. “It can be customized into any shape and color, making it imperceptible

or even stylish,” says KAUST Ph.D. student Abdullah Almansouri. The fabrication process is inexpensive and simple. “Anyone can start their own artificial skin project after a few minutes of training if they have the tools and materials,” he says. The team tested their magnetic skin for tracking eye movements by attaching it to an eyelid with a multi-axis magnetic sensor located nearby. Eye movement changed the magnetic field detected by the sensor whether the eyelid was opened or closed. The sensor can be incorporated into eyeglass frames or a sleeping mask or applied as an electronic tattoo on the forehead. It has potential for application as a human-com-

puter interface for people with paralysis or for gaming; for analyzing sleep patterns; or for monitoring eye conditions, such as drooping eyelids or driver alertness. The team also attached the skin to a latex glove fingertip and placed a sensor inside a light switch. When the magnetic skin comes close to the sensor—a distance that can be modified—the light switches on or off. This application could be especially relevant in laboratories and medical practices, where contamination is a concern. Kosel and his team are now extending the application so it can be used in a gesture-controlled wheelchair, a contact-free human-computer interface, and for noninvasive biomedical device localization. Almansouri, A. S., Alsharif, N. A., Khan, M. A., Swanepoel, L., Kaidarova, A., Salama, K.N. & Kosel, J. An imperceptible magnetic skin. Advanced Materials Technologies 4 (2019).

ABDULLAH ALMANSOURI PH.D. STUDENT Under the supervision of Jürgen Kosel, Abdullah is finding solutions for energy harvesting, digital and mixed-signal circuits and wirelessly powering devices.

Contamination can be avoided if laboratory equipment is controlled by the wave of a hand.

K AUST DISCOVERY

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Core Labs

IN THE GREENHOUSE, RESEARCHERS ASSESS ENTIRE PLANT HEALTH. If they are unsatisfied with the results, they revisit the lab, while a successful outcome moves the work toward field trials.

discovery.kaust.edu.sa 30

Spring 2020

A nanoscale optical chip developed by KAUST researchers could have widespread applications in natural hazard prediction and telecommunication networks.

PATTERNED OPTICAL CHIPS KEEP SECRETS PERFECTLY SAFE

Chaos could help put cyberhackers out of business with a patterned silicon chip that will be uncrackable even in the future. Confidential data—including credit card transactions and sensitive material in governmental institutions and military agencies—can be better protected during information exchanges through public channels. Andrea Fratalocchi led his student Valerio Mazzone and researchers in Scotland and a U.S. company to devise irreversibly modifiable silicon chips that emit chaotic light waves. The chips can make data encryption impossible to crack. Typical security protocols combine short public and private keys to encode messages. These protocols are fast but easy to crack because, while private keys are only known by senders and/or recipients, public keys are accessible to everyone. Quantum mechanics-based schemes offer a more secure and reliable alternative to

these protocols, but require more expensive and slower installations that are not scalable. “With the advent of faster and quantum computers, all classical schemes will be broken in a very short time, exposing the privacy of our present and, more importantly, past communications,” explains Ph.D. student Valerio Mazzone. An attacker can simply store an encrypted message sent today and wait for the right technology to become available to decipher the communication. The one-time pad has proven absolutely unbreakable. Its secrecy rests on a random, single-use private key that must be shared ahead of time between users. However, this key, which needs to be at least as long as the original message, remains difficult to produce randomly and send securely.

Fratalocchi’s team has developed an approach to implement this encryption technique in existing classical optical networks using patterned silicon chips. The researchers patterned the chips with fingerprints to obtain fully chaotic scatterers that cause mixed light waves to travel in a random fashion through these networks. Any modification, even infinitesimal, of the chips generates a scattering structure that is completely uncorrelated with and different from any previous one. Therefore, each user can permanently change these structures after each communication, preventing an attacker from replicating the chips and accessing the exchanged information. Moreover, these scatterers are in thermodynamic equilibrium with their environment. Consequently, an ideal attacker with unlimited technological power and abilities to control the communication channel and access the system before or after the communication cannot copy any part of the system without reproducing the surroundings of the chips at the time of the communication. “Our new scheme is completely unbreakable, no matter the time or the resources available, today or tomorrow.” Mazzone says. The researchers are currently working on developing commercial applications of this discovery. “Our team is searching for potential industrial partners and looking forward to implementing this system at the global scale. When this system is commercially released, all cyberhackers will have to look for another job,” Fratalocchi concludes. Di Falco, A., Mazzone, V., Cruz, A. & Fratalocchi, A. Perfect secrecy cryptography via correlated mixing of chaotic waves in irreversible time-varying silicon chips. Nature Communications, 10 (2019).

K AUST DISCOVERY

Cryptography is defined as the art of writing or solving codes.

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2019 ANDREA FRATALOCCHI

NOV EL M ATERI A L S

Spring 2020

FE AT URE

FOOD FOR THE FUTURE KAUST researchers are combining their efforts to improve food security sustainably. The global population is expected to reach 10 billion by 2050. With more than two billion people already lacking regular access to safe, nutritious and sufficient food, there is a significant challenge to feed our ever-growing human population. Director of the University’s Center for Desert Agriculture Rod Wing has made it his life’s work to help in the quest to feed 10 billion people. “The primary question for our lab is how can we grow enough food sustainably to feed 3 billion additional people by 2050?” says Wing. “Put another way: how can we feed the world without destroying our planet?” Rice, as a staple food for more than half the world’s population, is critical for food security. Much of Wing’s focus is on breeding green super rice1 varieties that produce larger and more nutritious yields with less water, fertilizer, pesticides and land. One of Wing’s projects is domesticating a wild relative of rice that can grow in saltwater. Another is analyzing the vast amount of genomic information available in cultivated and wild rice varieties and generating reference genomes that will eventually be used to create a digital gene bank. The computational biology group he is establishing will cross-reference the data from this bank with data on rice traits in order to accelerate the breeding of more resilient sustainable rice varieties. His colleague Mark Tester is sifting through barley, tomato and quinoa genome sequences to identify the genes that code for salt tolerance traits2. His team located genes responsible for salt stress tolerance in barley while studying a series of barley lines that were generated by crossing a

domesticated variety and several wild ones. They are now crossing these genes into commercial barley strains. The group’s work on the quinoa genome3 aims to breed stronger plants with better tasting seeds. Quinoa is recognized for its nutritious value, in addition to its ability to grow in salty soils and at high altitudes. Tester’s work could help breed quinoa as an alternative staple crop in foodinsecure countries. Tester’s group is also working on irrigating crops with partially desalinated water and on finding ways to reduce desalination costs to create an economically viable and sustainable irrigation system. Early success of this work spurred Tester to establish Red Sea Farms with agricultural engineer Ryan Lefers. Their company provides cuttingedge agricultural technologies to greenhouse and

3 150 30,000

Half human diet Commonly cultivated Edible

Of the roughly 400,000 plant species on Earth, about 7.5% are edible. Only about 0.5% of edible plants are commonly cultivated, and of those, 2% comprise 50% of our calorie intake in the form of wheat, maize and rice. Domesticating and cultivating more species of plants is an opportunity to increase global food production and meet growing demands for healthy food to feed a growing population.

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FE AT URE hydroponic farms for growing produce with less water and energy by using saltwater resources and cooling systems that utilize undiluted seawater. “I want to increase the sustainability of our food production systems and reducing freshwater use is one way to do this,” says Tester. “Security of food and water is incredibly important sociopolitically and environmentally. I can make a small impact on this, so I don’t want to waste that opportunity.” Matthew McCabe helps Tester gather data from thousands of individual plants using specially equipped unmanned aerial vehicles (UAVs) 4. McCabe also uses UAVs and shoebox-sized commercial satellites to monitor large-scale agriculture throughout the Kingdom of Saudi Arabia. His team analyzes the data to determine how much water is used to grow individual crops. “This is an incredibly useful tool that helps to manage the Kingdom’s precious water resources,” he explains. McCabe’s team is also involved in a Ministry of Environment, Water and Agriculture project that is mapping agricultural water use throughout the Kingdom. The data gathered by McCabe’s team from satellites and UAVs can help achieve precision agriculture, which enables farmers to identify and address problem areas in fields, saving money and resources, and growing better-quality crops. “But all these observational advances come with a massive increase in the amount of data being processed,” says McCabe. To tackle this challenge, he is employing machine learning techniques to extract information from their rich data sets that can then be used to guide the management and operation

Spring 2020

of agricultural systems. McCabe’s team is also looking for ways to integrate highresolution remote sensing data, weather forecasts, and state-of-the-art crop growth models to develop crop yield predictions and forecasting. “We’re trying to see if we can predict crop-yields weeks or months in advance of the actual harvest. These efforts have direct applications for food security because we currently lack the capacity to accurately forecast end-of-season yields.” Improving agricultural sustainability requires a strong foundational understanding of plant science. Ikram Blilou says her fundamental plant research is mainly curiosity driven. Her team wants to understand the biological processes involved in plant growth, with a focus on root systems. This work could lead to important applications. For example, Blilou and her team are investigating how specific plant genes are able to fine tune plant growth and determine their ability to defend themselves against pathogens, like the fungus Botrytis, which causes annual crop losses costing tens of billions of dollars. Blilou is also studying date palm genomes and is investigating how these plants cope5 with arid soils and high desert temperatures. She is hoping that this work will lead to knowledge that can optimize date palm growth and production, which could, in turn, be transferable to help other crops capture and retain water. Blilou was also involved in some of Salim Al-Babili’s fundamental plant research on the developmental role of

carotenoids, pigments with vital functions in photosynthetic organisms. Al-Babili and Blilou worked together on the discovery of zaxinone6, a carotenoid metabolite that improves cereal crop growth while also controlling crop infection with the menacing purple witchweed, Striga, which deprive their host crop of vital water and nutrients. Zaxinone suppresses the synthesis and release into the soil of plant hormones called strigolactones, thus preventing triggering the germination of the Striga seeds. Al-Babili is developing zaxinone analogs and other hormone-based products that can reduce Striga infestations, which cause more than US$7 billion worth of crop losses annually. Al-Babili has also discovered anchorene, a small carotenoid-derived metabolite that regulates the formation of plant anchor roots when the surrounding soil is deficient in nitrogen. In collaboration with Duke University, he also found that a small carotene-derived molecule, called beta cyclocitral7, is a root growth regulator that improves rice growth during salt stress. “It is basic research that will help us survive and meet future food challenges,” says Al-Babili. “There are many examples where basic research has heralded breakthroughs that have led to applications.” Al-Babili’s research has maintained a strong focus on translation to real-world

applications that benefit society. “It is exciting here at KAUST to have good experiments running, and at the same time, to see that they can be translated right away,” explains Al-Babili.

protective organogenesis in date palms: A

1. Wing, R. A., Purugganan, M. D., Zhang, Q.

zaxinone regulates growth and strigolactone

The rice genome revolution: from an ancient

biosynthesis in rice. Nature Communications

grain to green super rice. Nature Reviews

10, 819 (2019).

Genetics 19, 505–517 (2018).

7. Dickinson, A. J., Lehner, K., Mi, J., Jia K-P.,

2. Saade, S., Maurer, A., Shahid, M.,

Mijar, M., et al. β-Cyclocitral is a conserved

Oakey, H., Schmökel, S. M., et al. Yield-

root growth regulator. PNAS 116, 10563–

related salinity tolerance traits identified

10567 (2019).

morpho-devo-dynamic adaptive strategy during early development. The Plant Cell 31, 1751–1756 (2019). 6. Wang, J. Y., Haider, I., Jamil, M., Fiorilli, V., Saito, Y., et al. The apocarotenoid metabolite

in a nested association mapping (NAM) population of wild barley. Scientific Reports 6 (2016). 3. Maughan, P. J., Chaney, L., Lightfoot, D. J., Cox, B. J., Tester, M. et al. Mitochondrial and chloroplast genomes provide insights into the evolutionary origins of quinoa (Chenopodium quinoa Willd.) Scientific Reports 9, 185 (2019). 4. Johansen, K., Morton, M. J. L., Malbeteau, Y. M., Aragon, M., Al-Mashharawi, S. K. et al. Unmanned aerial vehicle-based phenotyping using morphometric and spectral analysis can quantify responses of wild tomato plants to salinity stress. Frontiers in Plant Science 10 (2019). 5. Xiao, T. T., Raygoza, A. A., Pérez, J. C.,

“H o w c a n we g r ow enough food sustainably to feed 3 billion additional people by 2 0 5 0 ? ”

Kirschner, G., Deng, Y. et al. Emergent

Studying how date palms cope with arid soils and high temperatures may also help understanding of how other crops capture and retain water.

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FE AT URE

Farming in the Desert A multidisciplinary effort for sustainable agriculture

Sensing technologies Using data collected by unmanned aerial vehicles (UAVs) and nanosatellites that indicate crop health, farmers can "farm smart," providing water and nutrients only to the areas in a field that need them.

CubeSat

Adaptations to the desert Studying desert plants, like the date palm, that thrive in harsh conditions can provide useful information on how to develop crops with higher stress tolerance and productivity.

New greenhouse technologies High-value, salt-tolerant crops are grown in diluted seawater in a greenhouse cooled using seawater with built-in humidity recovery systems.

Air in

Air out

Cooling, purification (seawater evaporation) Humidity control (liquid desiccant)

Suitable conditions

Germination pauses

Germination continues Palm tree seedling

UAV

Hydroponics

Harsh conditions

Humidity recovery

The future of plant domestication It took about 10,000 years for humans to domesticate maize. Genomics, bioinformatics and genome editing are tools that can be used to reduce the time needed for domestication to only about 10 years.

Resistance to disease Using genome editing techniques, researchers can confer leaf rust resistance to cereal crops to considerably increase crop yields.

Microbes Higher yields can be acheived by adding microbes, identified to promote plant growth or offer protection from abiotic stresses, to nutrient-poor soils.

Wheat leaf rust

Wheat with enhanced resistance

Undomesticated plant Fonio has some valuable characteristics, but it does not have the traits that would allow it to be used as a large-scale crop. For example, the plant commonly undergoes seed shattering, whereby its seeds randomly disperse.

Very high drought tolerance

Seed shattering Lacks erectness Too tall Nonuniform germination and maturation

AS THE HUMAN POPULATION continues to grow, likely

need to maximize the yields of currently domesticated crops by

reaching 10 billion by 2050, the demand for nutritious food will

protecting them against disease and parasites and to discover

also grow. What is more, we must increase our food production

opportunities to domesticate new crops that will thrive when

both sustainably and in a warming environment. To do this, we

irrigated with salty water in nutrient-poor soils.

Desalination The process of water desalination is energy consuming. Developing crops that thrive using partially desalinated water can save considerable amounts of energy.

Aquaculture Producing nutritious feed for fish and finding ways to adapt existing species of fish to better suit captive breeding will help to optimize outputs from aquaculture.

Salt-tolerant crops After identifying the genes that give wild species of plants salt tolerance, researchers can use genome editing to confer this trait to common cereal crops.

Defeating parasites Annual losses in cereal crop yields due to Striga infestation exceed US$7 billion. Understanding molecular pathways has helped to identify a technology to induce "suicidal germination" in this parasitic plant.

Salt water

Hydrophobic sand A thin layer of hydrophobic sand on the topsoil surrounding crops reduces water loss caused by evaporation.

Hydrophobic sand Striga seed

Genome editing

Germination

Withouth a host, the seed dies

More water available for the plant

1 Locate known gene 2 Identify corresponding gene in domesticated plant

The gene responsible for conferring a desirable trait in a domesticated plant can be identified and shared by targeting a Sh1 change to a single Responsible for nucleotide in the seed shattering genome of a related undomesticated plant. Sorghum DNA

in undomesticated plant

3 Target single-

nucleotide change

Fonio DNA

Domesticated plant Achieving an optimal crop plant requires continual improvements to increase yield, nutritional value and resistance to stress and disease.

Very high drought tolerance Mimimal seed shattering Erect Short Uniform germination and maturation

2019, KAUST; XAVIER PITA

Strigolactone analogs induce seed germination

FE AT URE

FEEDING THE WORLD SUSTAINABLY

The global food system is facing increasing pressures, including climate change, a growing population and greater political instability. BY SIR CHARLES GODFRAY

Today, there are approximately 7 billion people on Earth. By the middle of the century, that number will be nearer 10 billion. The good news is that the rate of population increase is declining. However, more resources will be required to produce the food needed to improve people’s diets as they come out of poverty. Thus, in the next few decades, we will see a substantial rise in the global demand for food. This rise in demand coincides with mounting pressure on the supply side of food production, with greater competition for land and water resources, for example. For decades, we have been overexploiting soils, which have lost fertility and depend on copious external inputs, such as water, fertilizers and insecticides. Also, the world is expected to face more frequent shocks: threats from climate change will inexorably increase, and we are seeing deepening political instability, in particular around international trade. It is especially clear, if you live in the Middle East, that a well-functioning global commodity trading system is essential to meet food demand.

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Much can be done to meet these challenges. We need to get serious about tackling climate change, an existential challenge to humanity in the 21st century. We must also stress test our international commodity trading system, checking its resilience the way we should have checked the global financial sector’s system in the early 2000s. Within the food system, we need to take action on agricultural production, diets and waste. We need to produce more food from essentially the same agricultural footprint, but with much fewer negative impacts on the environment. This is often called sustainable intensification. The alternative, extensification, is no longer a viable option. There is very little new land available for agriculture without hugely deleterious effects on greenhouse gas emissions and on biodiversity. Sustainable intensification has several components. We need crop and livestock varieties and breeds that are higher yielding, resource efficient and resilient to the shocks of climate change. Research at KAUST is important in this area—in particular its focus on waterefficient agriculture in arid regions. We need improved agronomy: systems for growing crops and rearing livestock that protect our soil and that also require less input from fertilizers, herbicides and insecticides. And we need to invest much more in agriculture in low-income countries, empowering smallholder farmers to produce—but sustainably—more food for themselves and for local and even more distant markets.

We’ll need to make difficult choices about the food we eat if we are to achieve a globally sustainable system. It is impossible for a global population of 10 billion people to consume the diets we currently enjoy in high-income countries. There is just not enough land, and the environmental consequences of producing so much food would be disastrous. Also, these high-income diets are making us ill. There is an epidemic of high body weight and obesity, with more diet-related illnesses associated with overconsumption compared with underconsumption. We need to alter many aspects of our diet. Eating less sugar and fat, for example, will improve our health, while consuming less meat is the best thing we can do for the environment. Finally, we need to waste less food. Estimates vary, but around one-third of all food produced is never eaten. In lowincome countries, the problems tend to be on the farm and in the food chain. In high-income countries, waste tends to be greatest in the home and in the eatingout sector. We need economic incentives to reduce waste, and changes to social norms so that it is no longer acceptable to throw food away. By the end of this century, human population numbers are likely to have plateaued and may even be going down. It is possible to feed that many people without wrecking the planet. But to do so, we need to act now. We need to invest much more in research on technical innovations for sustainable intensification, and we need the political will to make difficult decisions about climate change and diets. Sir Charles Godfray is the director of the Oxford Martin School and the Oxford Programme on the Future of Food. He is a population biologist with broad interests in the environmental sciences and has published in fundamental and applied areas of ecology, evolution and epidemiology. He is interested in how the global food system will need to change and adapt to the challenges facing humanity in the 21st century. In particular, he is interested in the concept of sustainable intensification, and the relationship between food production, ecosystem services and biodiversity.

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DATE PALMS PICKY ABOUT BACTERIAL PARTNERS

Cultivated date palms have co-evolved with desert bacteria for so long that their roots attract the microbes that provide the best chance for a long and healthy life.

The team found that the Sahara palm tree roots consistently associated with two types of bacteria.

They found that the soil directly attached to the date palm roots was significantly modified compared with the surrounding “bulk” soil.2 And even though the dominant bacterial species in bulk soil varied from one location to another, date palm roots consistently chose to associate with the same two types of bacteria: Gammaproteobacteria and Alphaproteobacteria. These bacteria provide important services to the date palms—they promote the secretion of an important plant growth hormone and provide a protective effect against stresses, like drought. “We hope that our study will lead to other microbial ecology studies on desert oasis ecosystems; one of the most productive, yet unique, agroecosystems,” says Mosqueira. The research group has several existing projects investigating desert plants and their associated microbiomes. A future focus will be to better understand the molecular interactions between plant roots and microbes as well as find ways to apply this knowledge to provide protective and nutritional services to agricultural crops grown in arid regions. 1. Marasco, R., Mosqueira, M. J., Fusi, M., Ramond, J-B., Merlino, G. Booth, J.M.,

Bacterial DNA sequencing analyses show date palms that are cultivated over a vast stretch of the Tunisian Sahara Desert consistently attract two types of growth-promoting bacteria to their roots, regardless of the location. This finding could help with improving crop cultivation in a warming climate. Many factors influence which growthpromoting bacteria associate with plant roots, including plant species, plant community diversity, agricultural practices applied and soil type. Research conducted on natural ecosystems shows that different types of wild plants attract different growth-promoting bacteria depending on their needs. Studies on conventional agricultural ecosystems have shown that plantroot-bacteria associations vary according to the type of soil and the agricultural practices applied. A KAUST study recently found that the roots of speargrass growing in the Tunisian desert are not picky at all: they attract whatever growth-promoting

bacteria they can find in the surrounding resource-poor sand.1 “But what happens in ecosystems where features of natural and agricultural environments converge, like in desert oases?” asks KAUST graduate Maria Mosqueira. “Under a climate change scenario, it is important to understand the role of microorganisms in arid ecosystems,” she explains. Mosqueira, and colleagues working with Daniele Daffonchio, conducted microbiome analyses to identify the types of bacteria associated with the roots of cultivated Deglet Nour date palms in seven oases distributed over a vast 22,200 square kilometer stretch of the Tunisian Sahara Desert. The oases were located in contrasting environments: on the seacoast, in the mountains, among sand dunes and in the saline soil regions of the northern edge of the Tunisian Sahara Desert. Analyses of the ribosomal RNA gene were also conducted to test for the types of bacteria present in the surrounding sand/soil.

Maggs-Kölling, G., Cowan, D. & Daffonchio, D. Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host. Microbiome 6 (2018). 2. Mosqueira, M. J., Marasco, R., Fusi, M., Michoud, G., Merlino, G., Cherif, A. & Daffonchio, D. Consistent bacterial selection by date palm root system across heterogeneous desert oasis agroecosystems. Scientific Reports 9 (2019).

MARIA MOSQUEIRA ALUMNA During her time in Daniele Daffonchio’s group, Maria’s research focused on characterizing the composition and the structure of underground microbiota— bacterial and fungal communities— associated with desert plants as well as the factors that shape these communities. Maria is currently working for a KAUST startup called Edama Organic Solutions, which develops and tests new agricultural products specifically designed to meet the needs of arid ecosystems.

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Striga Infestation STRIGA HERMONTHICA, also know as “purple witchweed,” is an invasive parasitic plant that siphons off water and nutrients from the host crop for its own growth. In sub-Saharan Africa, losses to cereal crop yields due to Striga infestation exceed US$7 billion, endangering the livelihoods and food supplies of an estimated 300 million people.

50 million ha of infested area

STRIGA INFESTATION IN AFRICA

40% yield losses up to complete crop failure

Heavy Moderate Light

$ 7–10 billion losses in cereal crops

The plant's delicate purple blooms disguise its devastating threat to the global food chain

How Striga infests crops DORMANT SEEDS

Debilitated adult host plant DEVELOPMENT

Striga seeds can lie dormant in the soil for up to 15 years, awaiting ideal growth conditions

GROWTH AND MATURATION

≈150 microns or the thickness of 2 sheets of paper

Young healthy host plant

EMERGENCE

CONDITIONING

The seeds become responsive to germination stimulants when the weather is warm and the soil is moist.

SEED PRODUCTION

A single plant can produce up to 100,000 seeds

Strigolactones Haustorium Host root ATTACHMENT

Nutrients flow from the host to the parasite

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HAUSTORIUM INITIATION

The haustorium allows Striga to attach itself to the host, forming a bridge between the two

O OH

O O

GERMINATION

Germination starts when the seed detects chemical signals released by the host, generally strigolactones

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Fighting the parasite “If you want to combat Striga, you have to deal with the seed problem.” — Salim Al-Babili

Researchers at KAUST and their collaborators have found that Striga seeds can be killed by inducing suicidal seed germination using strigolactone analogs. This technique combined with integrated farming practices can be effective in reducing the Striga seedbank.

SUICIDAL GERMINATION Having been tricked into germination by the strigolactone analogs, and without a host from which to draw water and Strigolactone analogs

nutrients, the seed eventually dies.

Seed death

Germination

INTEGRATED FARMING PRACTICES

Striga-infested crop field

Strigolactone

Staple crop

analogs

Seedbank greatly reduced

Crop rotation Fallow section

Year 1 Year 2

Researchers propose a crop rotation system in

Year 3

which strigolactone analogs are applied to the fallow section of the field. Over a few years, the

Year 4

Striga seedbank is expected to be drastically reduced or even entirely eliminated. 2019 KAUST; XAVIER PITA

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CONFERRING LEAF RUST RESISTANCE IN CEREAL CROPS

Identifying genes that confer resistance to leaf rust infections could help generate durably resistant cereal crops. Genes have been identified that confer resistance to multiple leaf rust species in barley. The findings by an international team led by KAUST researchers could transform the breeding of durable disease-resistant cereal crops and help support efforts to improve global food security. “Disease is the exception and resistance is the rule— most microbes do not make us or cereal plants sick,” says Simon Krattinger from the Center for Desert Agriculture. “This is called nonhost resistance—resistance of an entire species against all races of a pathogen. However, nonhost resistance in cereals is poorly understood.” The cereal-rust relationship is ideal for studying nonhost resistance because all cereals belong to the grass family, but each cereal crop species is infected by only one specific rust (for example, wheat leaf rust only infects wheat). There are molecular factors in barley that prevent wheat leaf rust from establishing colonies; thus, pinpointing the genes responsible for generating this molecular barrier to infection would be invaluable for breeders. “Importantly, nonhost resistance is more durable than host resistance—a plant’s innate immune system provides some protection, but only until pathogens evolve to evade it,” says Krattinger’s postdoc Yajun Wang. “Our biggest challenge was to identify the nonhost resistance genes in barley plants, especially given that barley’s genome is almost twice the size of the human genome.” All barley cultivars are resistant to leaf rusts of other

Spring 2020

cereals; therefore, there is no clear genetic variation within barley species that might indicate which genes are involved. KAUST’s collaborators in the Netherlands devised a novel method of narrowing the search. They infected 1733 barley cultivars with wheat leaf rust. Most plants were resistant, but a few lines developed hints of leaf rust at the seedling stage. This was not enough to create a full infection, but the team was able to crossbreed these lines to generate one line that was highly susceptible to wheat leaf rust. This was then crossed with a normal barley cultivar and analyzed to pinpoint the genetic variations conferring nonhost resistance. “Through extensive genome analysis, we found the genes that encode a protein receptor kinase to create a barrier to wheat rust in barley,” says Wang. “Transferring these genes into wheat could result in cultivars that are resistant to all races of wheat rust.” “This is a very promising strategy that could finally solve one of the biggest problems in global wheat production,” notes Krattinger. Wang, Y., Subedi, S., DeVries, H., Doornenbal, P., Vels, A., Hensel, G., Kumlehn, J., Johnston, P., Qi, X., Niks, R.E. & Krattinger, S.G. Orthologous receptor kinases quantitively affect the host status of barley to leaf rust fungi. Nature Plants 5, 1129–1135 (2019).

2019 SIMON KRATTINGER

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Leaf rust infects wheat plants, considerably reducing crop yield.

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USING AN EMBRYONIC PAUSE TO SAVE THE DATE A date palm seedling can pause its development to boost its resilience before emerging into the harsh desert environment.

Spring 2020

2019 VINICIUS LUBE

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2019 TINGTING XIAO

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Formation of organs in a protective structure during early stages of date palm development. Embryo within the seed (A), remote germination (B) and date palm forming a sheath that protects organs during early development (B, C).

Dates are one of the most significant fruit crops grown in the Middle East; however, little is known about how these resilient palm trees flourish in the high temperatures of desert habitats. Now, researchers have shown that date palms, after germination, can pause their early development within womb-like root structures in the soil, ready to grow when the environmental conditions are just right. “Date palms are of huge importance to desert agriculture, especially in Saudi Arabia, where they are considered as a symbol of vitality and prosperity,” says Ting Ting Xiao, who worked on the study with an international project team, under the supervision of KAUST’s Ikram Blilou. “Dates are known for their medicinal and nutritional values. In Europe, they are considered a delicacy, while in the desert they are a promising sustainable food source.” “Our research was driven by curiosity. While there have been genomic and tissue-culture studies of date palms, there are few studies on the plant’s embryo development and organ formation,” Blilou explains. Date palms employ a method of remote germination: rather than growing the first shoot and root right next to the seed and close to the surface of the soil, the whole seedling (root and shoot) remains within a multilayered root-like structure that buries deep into the soil to protect the young plant. “It is what happens during remote germination that really surprised and delighted us,” says Xiao. “Using a combination of state-of-the-art high-resolution imaging and molecular tools, we found that date palms can pause their development—rather like some animals whose pregnancy lies dormant until conditions are favorable.”

When the time is right, such as when soil temperature increases, the plant emerges with a fully developed leaf and delicate root system, thereby maximizing its nutrient and water uptake in harsh surroundings. “This is a real breakthrough in understanding plant adaptations to hostile desert environments,” says Blilou. “Our insights could have immediate use for growers, who can focus on the root system to screen for new cultivars. Ultimately, this knowledge could help us in the fight against desertification.” In a combined effort, KAUST plant science groups also plan to assess the genetic diversity of date palms in the Kingdom using genome resequencing as well as establishing breeding strategies for date palms. This work will contribute to improving date palm fruit production and quality for this important crop. Xiao, T.T., Raygoza, A.A., Perez, J.C., Kirschner, G., Deng, Y., Atkinson, B., Sturrock, C., Lube, V., Wang, J.Y., Lubineau, G., Al-Babili, S. Ramirez, L.A.C., Bennett, M. & Blilou, I. Emergent protective organogenesis in date palms: A morpho-devo-dynamic adaptive strategy during early development. The Plant Cell 31, 1751-1766 (2019).

Date palm fruits are important for many cultures, can grow to 21-23 meters tall and have a lifespan of more than

100 K AUST DISCOVERY

years.

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Researchers noted that the plants became more salt tolerant as the ear number per plant increased, but only up to a point.

TESTING BARLEY’S SALT TOLERANCE IS A NUMBERS GAME Factors influencing the tolerance of barley to saline soils have been uncovered using an advanced robust statistical technique.

Spring 2020

Plant scientists are striving to cultivate crops that can cope with saline soils in the hope that this may help feed the world’s growing population, particularly in the face of climate change. Now, KAUST researchers have applied a newly developed robust statistical technique to examine how different barley plant traits affect yields grown in saline and nonsaline conditions. “The problem with traditional regression analyses is that they focus on finding the average, or mean, of a given distribution,” says Gaurav Agarwal, who worked on the project under the guidance of his supervisor, Ying Sun, and in collaboration with plant scientists Stephanie Saade and Mark Tester. “In plant science, this incomplete picture can be frustrating because we’re often more interested in details at the extreme ends of the distribution and in what these data can tell us about optimizing crops,” says Agarwal. Furthermore, the barley genome is almost twice the size of the human genome. The two research groups turned to new advanced quantile regression techniques to analyze the traits that influence salt tolerance and yield in barley plants. The team modeled the saline and nonsaline conditions jointly, dividing the data into different “quantiles” to build a more detailed picture of the entire distribution. In this way, they could focus their analyses on those plant groups that displayed higher yields and greater tolerance and then examine the main influencing factors.

FE AT URE The team’s results provide interesting insights into barley’s responses and could inform future crop decisions, particularly in arid parts of the world.

“T h e b a r l e y g e n o m e

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is almost twice t h e s i ze o f t h e h u m a n g e n o m e.” Two key traits help gain high yield under saline conditions. Firstly, the plants’ flowering time should not occur too late in the growing season. Late flowering may mean that the plant is affected by increased heat as the season progresses, reducing its ability to produce seeds. “A more surprising result was that the salinity tolerance of plants increased linearly as the ear (grain-bearing part of a cereal plant) number per plant increased,” says Agarwal. “However, tolerance then faltered when a plant grew more than three ears. A possible explanation is that the plant can cope with salt stress while producing seeds, but only up to a point, after which generating seeds comes at the expense of salinity tolerance.” “We are keen to expand on these initial results,” adds Sun. “Our insights may also help further understanding of mechanisms of salt tolerance in barley and other crops.” Agarwal, G., Saade, S., Shahid, M., Tester, M. & Sun, Y. Quantile function modeling with application to salinity tolerance analysis of plant data. BMC Plant Biology 19 (2019).

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Data from the field trial is analyzed using an advanced robust statistical technique that can help to explore the influence of different plant traits on barley yield under saline and nonsaline conditions.

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KAUST SCIENTISTS PERFORM GENOME SEQUENCING TO IDENTIFY DESIRABLE PLANT TRAITS, such as salt, drought and disease tolerance, for transfer into a target crop plant using genome editing.

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PUSHING PEROVSKITE SOLAR STABILITY

Solar perovskite materials could be spiked with organic cation dopants to suppress decomposition and degradation. Expanding the list of organic ingredients that comprise perovskite solar materials could boost their long-term stability and performance, researchers have predicted. Perovskites have recently captured the limelight in solar materials research because they can harvest solar energy almost as efficiently as conventional silicon solar cells and can be cheaper and easier to produce. One area where perovskites still lag behind silicon is their long-term stability. Now, Udo Schwingenschlögl from the KAUST Solar Center and his Ph.D. student Aleksandra Oranskaia have found a possible solution. The most-studied perovskites for solar applications consist of a negatively charged lead-halide inorganic skeleton, partnered with positively charged organic cations like methylammonium (MA) or formamidinium (FA). These combine in a highly regular atomic arrangement. The lead halide component is mainly responsible for interacting with light, while the organic component plays a more supporting role, providing structural stability. However, the relatively poor stability of these materials still restricts their commercial development. Using computational modeling, Oranskaia and Schwingenschlögl

examined the organic component of solar perovskite materials, looking for ways to improve the stability of FA-lead halide perovskites. “Our motivation was to apply new computational methods to one of the hottest problems in the field of perovskite solar cells,” Oranskaia says. Experimental studies have shown that FA-based perovskites are more stable than MA. Therefore, the team first compared MA and FA bonding strengths, focusing on noncovalent forms of bonding, such as hydrogen bonding. They then looked at whether adding other organic “dopants” into the FA-lead halide perovskite structure could enhance stability even further. “We showed for the first time that the noncovalent bonding strength of organic cations can be used

to improve hybrid perovskite materials,” Schwingenschlögl says. Although covalent bonds are the strongest, other types, including hydrogen bonding and halogen bonding between the organic cation dopants and the lead halide component, help to stabilize the perovskite structure. “We show that doping with organic cations of the right volume and shape— those that bond more strongly than FA to the inorganic skeleton via hydrogen and halogen bonding—can stabilize the material,” Oranskaia says. Organic cations with covalently and noncovalently bound chlorine atoms or ions proved to be particularly effective: they helped to suppress damaging halide movements known as X-migrations. “This offers a strategy to boost the performance of lead halide solar cells,” Schwingenschlögl says. The team next plans to study the effects of noncovalent interactions on the phase stability of other solar-related materials, Schwingenschlögl adds. Oranskaia, A. & Schwingenschlögl, U. Suppressing X-migrations and enhancing the phase stability of cubic FAPbX3 (X = Br, I). Advanced Energy Materials 9, (2019).

Hybrid perovskites are an effective and relatively inexpensive solar cell material but lag behind silicon in terms of stability. The purple and black components represent the inorganic perovskite skeleton with incorporated organic cations.

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2019 NATURE; YOUSSEF KHALIL

VISUALIZING SCIENCE

SMART REACTIONS THROUGH ONLINE DESIGN OF CATALYTIC POCKETS Mapping the three-dimensional structure of catalytic centers helps to design new and improved catalysts.

theoretical chemists like herself. “Using the maps explains the importance of combining experimental and theoretical approaches better than my words have been able to do,” she observes. “They can be used with any class of catalyst, from reactivity promoted by simple organic molecules to that promoted by transition metal complexes and large metalloenzymes, where a metal is hosted inside a protein.” Metalloenzymes catalyze some of the most crucial reactions of life. Work at KAUST continues to enhance the method, including developing machine learning approaches to rapidly screen the potential of possible new catalysts. “This perspective article is important because it officially states the validity and value of the topic,” says Falivene. She describes it as a new starting point that brings together the early, less formal achievements to promote wider use and further development of the maps. Falivene, L., Cao, Z., Petta, A., Serra, L., Poater, A., Oliva, R., Scarano, V. & Cavallo, L. Toward the online computer-

Spring 2020

aided design of catalytic pockets. Nature Chemistry 11, 872-879 (2019).

This topographical steric map shows a ligand in its corresponding metal complex. Orange and blue zones indicate more or less hindered zones of the catalytic pocket, respectively.

LAURA FALIVENE RESEARCH SCIENTIST In Luigi Cavallo’s group, Laura uses computational techniques to rapidly screen novel catalyst architectures to obtain insights that could help in the design and experimental synthesis of novel and improved catalysts.

2019 LAURA FALIVENE

Many chemical processes depend on catalysts to facilitate reactions that would otherwise proceed very slowly, or not at all. An innovative procedure for visually representing the structure of catalysts via computer-assisted design is helping researchers build better catalysts. The software developed by Luigi Cavallo’s group generates topographic steric maps, for which the source code is now freely available online. Scientists from 65 countries have already used the interfaced web application, reports postdoctoral fellow Laura Falivene, and they often call on the KAUST researchers for more information. The team has now published a perspective article explaining in detail the creation and use of the topographic steric maps. “The power of visualization is of great value in chemistry where much time is spent imagining things that we cannot see,” Falivene says. Each map uses color coding to convey the threedimensional geometry of the chemical groups, forming the functional heart of a catalyst, known as the catalytic pocket. The data to build a map can come from several techniques, such as X-ray crystallography and quantum mechanics calculations, which indicate the identity and position of each atom in the catalytic pocket. This helps researchers better understand how known catalysts function, while also guiding exploration of chemical modifications that could adjust the structures to make better catalysts. “We are building an important bridge between experimental and computational approaches,” Falivene explains. She adds that the growing popularity of topographic steric maps helps other chemists to appreciate the significance of the work done by

Elhoseiny and Elfeki’s research aimed at developing what is called a zero-shot learning (ZSL) algorithm to help with the recognition of previously unseen categories based on class-level descriptions with no training examples. “We modeled the visual learning process for ‘unseen’ categories by relating ZSL to human creativity, observing that ZSL is about recognizing the unseen while creativity is about creating a ‘likable unseen’,” says Elhoseiny. In creativity, something novel but pleasing or “likable” must be different from previous art, but not so different as to be unrecognizable. In the same way,

“I m a g i n a t i o n i s o n e o f t h e ke y properties of h u m a n i n t e l-

AI USES YOUR IMAGINATION

ligence that enables us to understand the

The psychology of human creativity helps artificial intelligence imagine the unseen. By learning to deviate from known information in the same way that humans do, an “imagination” algorithm for artificial intelligence (AI) is able to identify previously unseen objects from written descriptions. The algorithm, developed by KAUST researcher Mohamed Elhoseiny in collaboration with Mohamed Elfeki from the University of Central Florida, paves the way for artificial imagination and the automated classification of new plant and animal species. “Imagination is one of the key properties of human intelligence that enables us not only to generate creative products like art and music, but also to understand the visual world,” explains Elhoseiny. Artificial intelligence relies on training data to develop its ability to recognize objects and respond to its environment. Humans also develop this ability through

accumulated experience, but humans can do something that AI cannot. They can intuitively deduce a likely classification for a previously unencountered object by imagining what something must look like from a written description or by inference from something similar. In AI, this ability to imagine the unseen is becoming increasingly important as the technology is rolled out into complex real-world applications where misclassification or misrecognition of new objects can prove disastrous. Also important is the sheer volume of data needed to reliably train AI for the real world. It is unfeasible to train AI with images of even a fraction of the known species of plants and animals in the world in all their permutations, let alone the countless undiscovered or unclassified species.

v i s u a l wo r l d .” Elhoseiny and Elfeki carefully modeled a learning signal that inductively encourages deviation from seen classes, yet not pushed so far that the imagined class becomes unrealistic and loses knowledge transfer from seen classes. The resultant algorithm showed a consistent improvement over the state-of-the-art benchmarks for ZSL. “One of the possible applications of our approach is in identifying unseen species,” says Elhoseiny. “AI that is powered with this technology could help report species sightings without pictures, just with language descriptions.” Elhoseiny, M & Elfeki, M. Creativity inspired zero-shot learning. arXiv preprint The IEEE International Conference on Computer Vision (ICCV) (2019).

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2019 NATURE; YOUSSEF KHALIL

VISUALIZING SCIENCE

SPOTTING CANCERâ&#x20AC;&#x2122;S GREASY FINGERPRINTS Laser-based microscopes can tune into multiple biomolecular signatures found in cancer cells.

Spring 2020

Lipid droplets normally involved in storing fats have recently been revealed as key players in many cancer cell processes, including their ability to resist treatment. These lipids can now be quantitatively identified more easily than ever using a microscopy technique developed at KAUST. The chemical bonds holding molecules together produce unique vibrations when excited by a light source. Researchers are now exploiting this effect to characterize living cells and tissue through stimulated Raman scattering microscopy. In this approach, ultrafast laser pulses are used to vibrate biomolecules throughout the volume of a sample. The resulting signals can then help visualize components, including lipids at speeds suitable for video imaging. One challenge with stimulated Raman scattering involves collecting data from two significant parts of

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“We a r e i n t e r e s t e d in seeing how these droplets change when ex p o s e d t o c o n d i t i o n s , s u c h a s c h e m o t h e ra p e u t i c a g e n t s .”

the molecules’ vibrational spectrum: a “C-H stretch” region, where hydrocarbon bonds elongate, and a “fingerprint” region, involving bond bending and twisting. Typically, researchers must take multiple measurements of each spectral zone with different optical components—a cumbersome process. “The fingerprint region is the richest in detail that can reveal molecular structures, especially when it can be correlated with C-H stretch information,” explains bioscientist Siarhei Laptenok, a postdoc in Carlo Liberale’s group. “It’s critical to have the capability of collecting rapidly from both regions with a single measurement.” To speed up the vibrational measurements, Liberale’s team incorporated an electronically tunable optical filter into their microscope. The filter selects the beam’s emissions on a very fast time scale that minimizes the need to perform time-consuming steps, such as changing or realigning optical components of the microscope. In this way, there is a dramatic fall in time for a typical highresolution scan across the two main regions, from minutes to seconds, while retaining high spectral resolution. To demonstrate the biomedical potential of their microscope, the KAUST team collected vibrational data on human liver cancer cells. Selecting laser light that stimulates lipids enabled the researchers to produce images of the cancer cell that spotlight the tiny internal regions housing high concentrations of fat molecules through specific vibrational fingerprints. Other experiments also revealed the microscope could differentiate fats based on their saturated hydrocarbon content. “Being able to see lipid droplets with great resolution and detail is really exciting, especially because it has only just come to light that cancer cells metabolize lipids in abnormal ways,” says Liberale. “We are interested in seeing how these droplets change when exposed to conditions, such as chemotherapeutic agents.” Laptenok, S.P., Rajamanickam, V.P., Genchi, L., Monfort, T., Lee, Y., Patel, I., Bertoncini, A. & Liberale, C. Fingerprintto-CH stretch continuously tunable high spectral resolution stimulated Raman scattering microscope. Journal of Biophotonics (2019).

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2019 ANDREA BERTONCINI

Stimulated Raman microscopy of lipid droplets. Two laser beams with different colors nonlinearly interact inside the lipid droplet. The variation in their intensity holds chemical information.

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MASTERING A PRICKLY PROBLEM IN FERROFLUIDS

Computer simulation accurately captures the beguiling motion of a liquid magnetic material.

models, Huang says. Previous models typically handled magnetic-field simulation using magnets that are infinitely small. The closer two magnets are brought together, the stronger the magnetic attraction—thus, if a magnet is infinitely small, the magnetic field strength can become infinitely large. “The center of an infinitely small magnet is called its singularity,” Huang says. Not only is the magnetic field difficult to measure at the magnet’s center, but if two singularities come close together, the forces become so large that the simulation can crash. “We derived formulas to eliminate the singularities and to create more robust numeric schemes,” Huang says. The team also found ways to increase computational efficiency by reducing the algorithmic complexity, allowing larger simulations to be run. When the team compared their model with wet lab experiments, it reproduced the true dynamic behavior of the ferrofluid, giving a good qualitative representation that will be useful for ferrofluid sculpture design. “This opens the door for further quantitative analysis,” Huang says. Increasing the model’s accuracy further would provide new insights into fundamental ferrofluid behavior and lead to many new uses, from electronic sensors and switches to deformable mirrors for advanced telescopes.

Ferrofluids, with their mesmeric display of shapeshifting spikes, are a favorite exhibit in science shows. These eye-catching examples of magnetic fields in action could become even more dramatic through computational work that captures their motion. A KAUST research team has now developed a computer model of ferrofluid motion that could be used to design even grander ferrofluid displays. The work is a stepping stone to using simulation to inform the use of ferrofluids in a broad range of practical applications, such as medicine, acoustics, radar-absorbing materials and nanoelectronics. Ferrofluids were developed by NASA in the 1960s as a way to pump fuels in low gravity. They comprise Huang, L., Haedrich, T. & Michels, D. L. On the accurate nanoscale magnetic particles of iron-laden comlarge-scale simulation of ferrofluids. ACM Transactions on pounds suspended in a liquid. In the absence of a Graphics 38 (2019). magnetic field, ferrofluids possess a perfectly smooth surface. But when a magnet is brought close to the ferrofluid, the particles rapidly align with the magnetic field, forming the characteristic spiky appearance. If a magnetic object is placed in the ferrofluid, the spikes will even climb the object before cascading back down. B ecause ferrofluid behavior can be counterintuitive, simulation is the ideal way to understand the complex motion. Until now, however, the models have had several limitations, says Libo Huang, a Ph.D. student in Dominik Michels’ group in KAUST’s Visual Computing Center. The first challenge was to eliminate singularities in the magnetic field of existing Exposing ferrofluids to a magnet gives them their unique spiky shapes.

Spring 2020

Yuan Wang (left), Hernando Ombao (right) and colleagues have developed a method that could provide a clinically useful tool for seizure localization.

EPILEPSY STUDY SHOWS THE SHAPE OF THINGS TO COME Pyramidal graphs resulting from statistical analyses of EEG recordings can improve our understanding of epileptic seizures. A statistical approach squeezes more detailed information out of a current method of measuring brain signals in epileptic seizures, adding new insight into how these signals originate and spread. Visual inspection of electroencephalography (EEG) recordings of epilepsy patients before and during a seizure is a fairly effective method for detecting the part of the brain that can benefit from surgical treatment. But it is not sufficient for more challenging cases. Now, an approach developed by KAUST biostatistician Hernando Ombao and colleagues Yuan Wang of the University of Wisconsin–Madison and Moo K. Chung of the University of California, Irvine, digs deeper into the features of an EEG and can detect abnormalities in brain

regions even before a seizure takes place. The method could provide a clinically useful tool for seizure localization, according to Chung and Wang. The approach stems from a field of mathematics that analyzes large and complex datasets by studying shape representations of the data and its interactions. Analyzing these shapes provides information on patterns that exist within the data. The team applied their method, known as a topological data analysis framework, to see what they could learn from an EEG recording conducted before and during an epileptic seizure. The statistical approach removes noise from the EEG recording, providing cleaner signals. Shapes are then drawn that directly relate to the signals in the recordings. The final pyramidal shapes (persistence

landscapes) that represent the signals coming from each electrode placed on the scalp provide a good picture of where the seizure originates in the brain and how it spreads. The analysis of the patient’s EEG recording showed that the seizure originated from a region in or around the electrodes measuring signals from the left temporal lobe of the brain. It then spread to the right temporal lobe. Further simulation studies showed that the test was robust and sensitive, even when the signal was buried under noise. “Epileptologists should enhance their toolboxes of data analysis by adding methods like this one that capture topological features as part of their assessment of seizure foci in more challenging cases of epilepsy,” says Ombao. The team next plans to test their framework on large samples of EEG recordings to clinically validate their findings. Ombao is also developing statistical methods to study the impact of shocks to the brain, such as in epilepsy or stroke, on the communication network between brain regions and nerve cell populations. Wang, Y., Ombao, H. & Chung, M. K. Topological data analysis of single-trial electroencephalographic signals. The Annals of Applied Statistics 12, 1506–1534 (2018).

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Manal Zaher reports that their hypothesis predicted the outcome correctly more than 90 percent of the time.

GLOWING RESULTS FOR SINGLEMOLECULE IMAGING

New experimental insights allow researchers to probe protein-DNA interactions with greater precision.

Spring 2020

A single-molecule imaging technique, called protein-induced fluorescence enhancement (PIFE), has gained traction in recent years as a popular tool for observing DNA-protein interactions with nanometer precision. Yet, according to a new KAUST study, research laboratories have not been using the technique to its fullest potential. The PIFE assay is predicated on the idea that DNA tagged with a fluorescent dye will glow brighter when proteins are bound in the vicinity. In many instances, this is true, which has led many scientists to adopt PIFE over other more laborintensive techniques that rely on dual labeling of proteins and DNA. But Samir Hamdanâ&#x20AC;&#x2122;s graduate students Fahad Rashid, Manal Zaher and Vlad-Stefan Raducanu realized that protein binding to DNA-dye complexes could sometimes have the opposite effect as well. Instead of enhancing the fluorescent signal, protein interactions can sometimes dampen the glow, depending on certain properties of the system.

VISUALIZING SCIENCE

“We t u r n e d e v e r y measurement into a g a m e.” Hamdan credits the curiosity of his students for making this observation and detailing how it works. Inspiration from Rashid’s previous work led the team to the phenomenon they call protein-induced fluorescence quenching (PIFQ). And as Rashid explains, “We set out to better define the conditions that lead to fluorescent booms or busts.” Through a combination of experimental and computational analyses, the team showed that the initial fluorescence state of the DNA-dye complex determines whether PIFE or PIFQ will result after protein binding. Without this knowledge, the likelihood of either event becomes equivalent to a coin toss, which can jeopardize the mechanistic interpretation of laboratory results. “When insight into this initial state is gleaned from fluorescence and structural work, the anticipation of either effect becomes experimentally feasible,” Raducanu explains. Factors such as DNA sequence and dye position could tip the balance toward PIFE or PIFQ; the team got so good at interpreting the molecular code that they could accurately predict which would happen simply by measuring how these parameters influence the initial fluorescence state of the DNA-dye system. “We turned every measurement into a game,” Zaher says, “And we are happy to say that our hypothesis predicted the outcome more than 90 percent of the time!” These novel insights should dramatically expand the reach and experimental promise of this powerful singlemolecule imaging tool, predicts Raducanu. “By introducing PIFQ, we offer researchers in the field the possibility to address several biological questions where PIFE might not have been witnessed,” he says. Scientists may also opt to combine PIFE and PIFQ to decipher multistep and multiprotein processes with just a single DNA-dye construct. “By taking into consideration the context-dependent nature of fluorescence modulation in the DNA-dye system, we open the door to many possibilities in experimental design that could be tailored to researchers’ needs,” Zaher says. “We now anticipate that interpretation of data and attribution of molecular events from single-molecule data will become easier and more precise,” Rashid adds. Rashid, F., Raducanu, V.S., Zaher, M.S., Tehseen, M., Habuchi, S. & Hamdan, S.M. Initial state of DNA-Dye complex sets the

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stage for protein induced fluorescence modulation. Nature Communications 10 (2019).

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GENE TWEAKING

AI REVEALS NATURE OF RNA-PROTEIN INTERACTIONS A deep learning tool could help in structure-based drug discovery. A new computational tool developed by KAUST scientists uses artificial intelligence (AI) to infer the RNA-binding properties of proteins. The software, called NucleicNet, outperforms other algorithmic models of its kind and provides additional biological insights that could aid in drug design and development. “RNA binding is a fundamental feature of many proteins,” says Jordy Homing Lam, a former research associate at KAUST and co-first author of the study. “Our structure-based computational framework can reveal the detailed RNAbinding properties of these proteins, which is important for characterizing the pathology of many diseases.” Proteins routinely interface with RNA

molecules as a way to control the processing and transporting of gene transcripts, and when these interactions go awry, information flow inside the cell is disrupted and disorders can arise, including cancer and neurodegenerative diseases. To better understand which parts of an RNA molecule tend to bind on different surface points of a protein, Lam and his colleagues turned to deep learning, a type of AI. Working in the laboratory of KAUST Professor Xin Gao in the Computational Bioscience Research Center, Lam and Ph.D. student Yu Li taught NucleicNet to automatically learn the structural features that underpin interactions between proteins and RNA. They trained the algorithm using threedimensional structural data from 158 different protein-RNA complexes available on a public database. Pitting NucleicNet against other predictive models—all of which rely on sequence inputs rather than structural information—the KAUST team showed that the tool could most accurately detect which sites on a protein surface bound

to RNA molecules. What is more, unlike any other model, NucleicNet could predict which aspects of the RNA molecule were doing the binding: part of the sugar-phosphate backbone or one of the four letters of the genetic alphabet. In collaboration with researchers in China and the United States, Lam, Li, and Gao validated their algorithm on a diverse set of RNA-binding proteins, including proteins implicated in gum cancer and amyotrophic lateral sclerosis, to show that the interactions deduced by NucleicNet closely matched those revealed by experimental techniques. “Structure-based features were seldom considered by other computational frameworks,” says Lam. “We have harnessed the power of deep learning to infer those subtle interactions.” NucleicNet is openly available for researchers who want to predict RNAbinding sites and binding preference for any protein of interest. The software can be accessed at http://www.cbrc.kaust.edu.sa/ NucleicNet/. Lam, J.H., Li, Y., Zhu, L., Wei, J.N., Umarov, R., Jiang, H., Heliou, A., Sheong, F.K., Liu, T., Long, Y., Li, Y., Fang, L., Altman, R.B., Chen, W. Huang, X, Gao, X. A deep learning framework to predict binding preference of RNA constituents on protein surface. Nature Communications 10 (2019).

The RNA interaction surface of Fem-3binding-factor 2 as predicted by NucleicNet.

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Stefan Arold (left) and Umar Hameed examine a plate of gut-dwelling bacteria. They hope to better understand how these bacteria cause diarrheal disease.

TURNING UP THE HEAT ON PATHOGENIC BACTERIA Protein found in gut-dwelling pathogens changes shape under human body temperatures, leading to toxins responsible for diarrheal disease. Pathogenic bacteria come alive at the metabolic level when they enter the warmth of the human gut, firing up genes that encode toxins and other compounds harmful to our bodies. A KAUST-led study shows how a critical bacterial protein senses changes in temperature to slacken DNA strands and boost gene expression in diarrhea-inducing bugs. “Having determined how these bacteria sense that they are inside humans, we could try to conceive of small molecules to perturb this mechanism,” says research scientist Umar Hameed. “Such compounds would block bacteria from adapting to their environment, which would weaken them and facilitate eliminating them.” Gut-dwelling bacteria that cause foodborne illnesses, including Salmonella, disease-causing strains of E. coli, and the cholera pathogen Vibrio cholerae, all use a protein called H-NS to condense their DNA and broadly restrict gene expression. Short for histone-like

nucleoid-structuring protein, H-NS forms multiunit complexes that help the microbes stay relatively dormant when free-floating in the environment. However, these complexes must break up for the protein to release its grip on DNA, which then allows the bacteria to thrive within a warm-blooded host, explains group leader Stefan Arold. Before coming to KAUST, Arold, who has studied H-NS for more than 15 years, previously determined the three-dimensional shape of part of the protein. While he had shown that its complexes collapse at human body temperature, it was not clear how that happened. In his lab at KAUST with colleagues Łukasz and Mariusz Jaremko, Arold and Hameed have now combined structural and biophysical experiments. This has enabled them to identify the exact part of H-NS, dubbed site2, that changes its conformation in response to a temperature rise, prompting the protein complexes to fall apart.

Computer simulations, performed with KAUST colleague Xin Gao and Jianing Li at the University of Vermont helped Arold’s team deepen these insights. Ultimately, they demonstrated that the partial disassembly of H-NS complexes leads the protein to adopt a self-inhibiting form that also blocks its ability to bind and recognize DNA. Arold and his team now hope to develop drugs that can stabilize the connection between proteins at human body temperature and prevent H-NS complexes from fragmenting. “If we can find compounds that reinforce the structure against heatinduced unfolding, then bacteria would not express toxins anymore; they would remain inoffensive and be generally weakened inside humans,” Arold says. Shahul Hameed, U.F., Liao, C., Radhakrishnan, A.K., Huser, F., Aljedani, S.S. Arold, S.T. H-NS uses an autoinhibitory conformational switch for environmentcontrolled gene silencing. Nucleic Acids Research 47, 2666-2680 (2019).

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Risk of contracting diarrheal disease can be greatly reduced by access to safe drinking water and use of sanitary practices.

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REGULATOR OF PLANT IMMUNITY TAGGED

Discovery of signaling intermediary could lead to more pest-resistant crops.

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“T h e n ex t s t e p i s t o t e s t our findings in crops by g e n e ra t i n g k n o c ko u t m u t a n t s .” A new actor in the immune system of plants has been identified. KAUST scientists now show that the protein MAP4K4 is needed to mount proper defenses against environmental pathogens. The discovery helps explain the tight control of immune signaling in plants and reveals targets in a molecular pathway that could be manipulated by crop breeders. “Our findings are directly applicable to making plants more resistant to pathogens,” says study author Heribert Hirt, professor of plant science at KAUST’s Center for Desert Agriculture.

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Yunhe Jiang (left) and Heribert Hirt check their plants for signs of disease.

MAP4K4 (short for mitogen-activated protein kinase kinase kinase kinase 4) is a well-established player in human immunity and inflammation, but its role in plant disease resistance was unknown. Hirt and his collaborators stumbled upon it during a large screen for proteins involved in signal transduction in the weedy thale cress Arabidopsis. By studying mutant plants that lack a working copy of MAP4K4, Hirt’s team then drilled down into the core functions of this protein. First, they showed that MAP4K4 was essential for proper immune responses to flg22, a peptide derived from a bacterial protein found within the filamentous flagellum of disease-causing microbes. Working with colleagues in France, the KAUST researchers—led by Hirt and postdoctoral fellow Yunhe Jiang—then detailed how. They demonstrated that MAP4K4 directly adds chemical tags (in the form of phosphate groups) at several sites of another protein, BIK1. These tabs help stabilize BIK1 and promote the production of highly toxic molecules that play a central role in pathogen resistance, explains Jiang. The researchers also showed that MAP4K4 tags a repressor of BIK1 with phosphate decorations. This chemical adornment disables the negative regulator to further promote BIK1 activation.

So far, Hirt and his group have only described this function of MAP4K4 in Arabidopsis immunity. “The next step is to test our findings in crops by generating knockout mutants,” Hirt says. “This is quite feasible now by using CRISPR-Cas9 geneediting technology that is established in tomato, rice and other species of agricultural importance.” The researchers also plan to examine the roles of other regulatory proteins within the MAP4K family, of which at least 10 exist in plants. Intriguingly, Jiang showed that one family member, MAP4K3, seems to act synergistically with MAP4K4 to control BIK1 stabilization and pathogen-induced immune responses. Closely related MAP4K proteins may thus share overlapping functions but also have distinct features that collectively contribute to the fidelity of immune signaling in plants. A better knowledge of these signaling mechanisms could help agribusinesses keep plant pathogens at bay. Jiang, Y., Han, B., Zhang, H., Mariappan, K.G., Bigeard, J., Colcombet, J., Hirt, H. MAP4K4 associates with BIK1 to regulate plant innate immunity. EMBO Reports 20 (2019).

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CHLORINE COULD INCREASE ANTIMICROBIAL RESISTANCE Ultraviolet light could thwart antimicrobial resistance by

Researchers recovered and isolated bacterial isolates from water samples collected from a local wastewater treatment plant.

damaging DNA material in wastewater. Conventional wastewater disinfection using chlorine could facilitate the spread of antimicrobial resistance in bacteria1. Treating some types of wastewater with ultraviolet (UV) light instead could be part of the solution2, according to a study at KAUST’s Water Desalination and Reuse Center, published in the journal Environmental Science & Technology. Bacteria are rapidly developing mechanisms to evade the effects of antimicrobial drugs, and this resistance is increasingly threatening public health. Pharmaceutical compounds and resistant bacteria that reach municipal and agricultural wastewater are partially to blame. Interestingly, the antimicrobial resistance of bacteria in wastewater entering water treatment plants is lower than after the wastewater leaves the treatment plant. This may be because during wastewater disinfection, genetic material breaks out of bacteria into the surrounding water. This extracellular DNA can contain antimicrobial resistance genes. “The big question is are these extracellular resistance genes of concern to public health?” says KAUST postdoctoral fellow, David Mantilla-Calderon. “We don’t have an answer to this question yet, but the first prerequisite these genes must fulfill to be of concern is that they need to be harbored within a viable bacterial cell.

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This is only possible through a process called natural transformation, which allows extracellular DNA uptake and integration into the bacterial chromosome.” Mantilla-Calderon and colleagues at KAUST found1 that natural transformation was stimulated in a bacterium commonly found in water and soil, called Acinetobacter baylyi, when it was in the presence of the chlorine byproduct, bromoacetic acid. They found that this disinfection byproduct caused DNA damage in the bacterium, inducing a DNA repair pathway that is known to also increase the integration of foreign DNA into the bacterium’s genome. Ph.D. student Nicolas Augsburger next investigated2 the effects of sunlight and one component of sunlight, UV light, on natural transformation. “We wanted to see if there was a safer way to disinfect treated wastewater without provoking an increase in natural transformation in environmental bacteria,” he explains. Interestingly, Augsburger and his colleagues found that, similar to bromoacetic acid, treatment with either the full spectrum of sunlight or only with UV light caused increased natural transformation in Acinetobacter baylyi. “What surprised us was the finding that after treatment with UV light, the bacterium’s genes were damaged to the

extent that they were no longer functional,” says Augsburger. “Thus, although treatment with UV light increased the integration of foreign DNA into the bacterium, just like disinfection byproducts and sunlight, it will not be able to express those genes.” “Our studies question our current reliance on the use of chlorine as the final disinfection step in most wastewater treatment plants,” says microbiologist Peiying Hong, who supervised the studies. “A disinfection strategy using UV light could be considered for disinfecting low turbidity water. This could help in minimizing wastewater contribution to antimicrobial resistance.” Hong’s lab is now investigating how various stressors might interact to affect uptake and integration rates of extracellular DNA into bacteria. 1. Mantilla-Calderon, D., Plewa, M. J., Michoud, G., Fodelianakis, S., Daffonchio, D. & Hong, P-Y. Water disinfection byproducts increase natural transformation rates of environmental DNA in Acinetobacter baylyi ADP1. Environmental Science & Technology 53, 6520–6528 (2019). 2. Augsburger, N., Mantilla-Calderon, D., Daffonchio, D. & Hong, P-Y. Acquisition of extracellular DNA by Acinetobacter baylyi ADP1 in response to solar and UV-C254nm disinfection. Environmental Science & Technology 53, 10312–10319 (2019).

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ARGONAUTE PROTEINS HELP FINE-TUNE GENE EXPRESSION

A protein, with a name reminiscent of legendary Greek sailors, has an unexpected role inside the human nucleus.

“Change s in the o rganization of chrom atin st r ucture can lead to abnormal character i stics in an o rganism and to d i seases.”

the dynamics of chromatin organization, and their contribution to gene regulation are largely unknown. Shuaib says that the group’s work not only establishes AGO1 as a new player in the study of 3D chromatin organization, “but also creates a paradigm for future investigations of the nonconventional role of RNA interference components in the nucleus.” Next, the team plans to study how AGO1 associated with nonprotein-coding RNAs maintains chromatin organization and how its depletion affects the outcome of gene copying inside the nucleus. Shuaib, M., Parsi, K., M., Thimma, M., Adroub, S., A., Hideya, K., Seridi, L., Ghosheh, Y., Fort, A., Fallatah, B., Ravasi, T., Carninci, P. & Orlando, V. Nuclear AGO1 regulates gene expression by affecting chromatin architecture in human cells. Cell Systems 9, 1–13 (2019).

2019 KAUST; HENO HWANG

A nuclear protein bound to RNA molecules affects chromatin structure and gene expression. Argonaute proteins (AGO) that are bound to RNA are known to play a role in RNA interference inside the cytoplasm. Despite their known presence in the nucleus, AGO’s role there is not clear. Now, environmental epigeneticist Valerio Orlando, his team at KAUST and colleagues in Italy and Japan, have uncovered the role of Argonaute proteins in the nucleus, using a combination of genomewide approaches. One of the four known Argonaute proteins, AGO1, was found to be present in the nucleus and was more prevalent than other Argonaute proteins on chromatin, the nuclear material that is composed of DNA and its associated network of molecules. AGO1 was found to bind to “enhancer” regions on DNA that are responsible for making sure that the right genes are expressed at the right time. This binding was mediated by long nonprotein-coding RNA molecules, called enhancer RNAs. Turning off AGO1 in human cells led to extensive changes in the gene expression program. It also led to changes in enhancer RNA levels, in the shape of chromatin, and in how its different parts interact. “The effect of AGO1 on 3D genome architecture was unexpected,” says KAUST epigeneticist Muhammad Shuaib. “Current advances suggest that changes in the organization of chromatin structure can lead to abnormal characteristics in an organism and to diseases,” explains Shuaib. “But the factors involved in establishing and maintaining this architecture,

Epigenetics examines how our cells acquire a memory that is shaped by their environment.

Normal gene expression (left): the enhancer-associated AGO1 helps maintain 3D chromatin organization. Perturbed gene expression (right): turning off AGO1 in human cells changes how chromatin loops interact and perturb gene expression.

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DATABASE TO SUPPORT INFECTIOUS DISEASE RESEARCH Linking disease pathogens to clinical signs and symptoms through a database could support research into the molecular mechanisms of infectious diseases.

infectious diseases and their associated pathogens. Finally, it includes information on known mechanisms of drug resistance for 30 pathogens. “This will interest clinical infectious disease investigators and the bioinformatics community; particularly the latter as the database brings together data in a way that can be readily shared, integrated and computed upon,” says Schofield. “This mobilization of data, particularly from a manually validated and curated database, can provide inputs into many projects. We sow the seeds and wait for the flowers to grow!” “PathoPhenoDB is a community resource and will evolve with the demands of the scientific community,” adds Kafkas. The team plans to keep the database up to date through regular repeats of their automated workflows. It also aims to include next-generation sequencing data for pathogens, which could help improve infectious disease diagnosis and treatment.

A new database PathoPhenoDB faciliPathoPhenoDB,” says Paul Schofield, a tates the search for associations between reader in biomedical informatics at the infectious diseases, the pathogens that University of Cambridge. cause them, the resulting clinical signs PathoPhenoDB is unique in that it links and symptoms, and the drugs that can pathogens to disease phenotypes: the clinitreat them. It also contains information cal signs and symptoms of disease. “Pheon the proteins and genetic changes that notypes encode for the molecular and can make pathogens resistant to treatment physiological mechanisms underlying with certain drugs. disease and can therefore be used to study Developed by researchers at KAUST these mechanisms,” says KAUST’s Robert in collaboration with the University of Hoenhdorf, who led the initiative. Cambridge, PathoPhenoDB can help The database is publicly accessible and infectious disease diagnosis and treatsearchable from http://patho.phenomKafkas, S., Abdelhakim, M., Hashish, ment, in addition to the study of the ebrowser.net/. A search term can be a Y. Kulmanov, M. Abdellatif, M. molecular mechanisms behind pathopathogen, disease, or disease phenotype. Schofield, P.N. & Hoehndorf, R. gen-host interactions. PathoPhenoDB currently covers assoPathoPhenoDB, linking human “Several databases already exist for infecciations between 508 infectious diseases pathogens to their phenotypes tious disease research,” says research scienand 692 taxa of pathogens. It also includes in support of infectious disease tist Şenay Kafkas. “But these either cover information about drugs that can treat 130 research. Scientific Data 6 (2019). part of the data available in our database, like including only disease-pathogen associations, or they focus on different aspects of the diseases, like host-pathogen interactions for understanding the disease mechanism.” To put together a comprehensive database, the team collected data from existing databases and then used artificial intelligence to automatically identify more information from the literature, explains Kafkas. The team’s clinical geneticist, Marwa Abdelhakim, then manually combed through the data for an accuracy check, adding or removing information where needed. “The group’s combination of computational, clinical and biological expertise put it in Robert Hoehndorf (left) and Senay Kafkas have developed a database that links disease pathogens to clinical signs and symptoms. a strong position to generate

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“To combat Striga, we need to get to the root of the problem. Destroying the seeds in the soil is the first step to eradicating this parasitic plant, which is strangling the water and nutrients from our food crops.”

Destination KAUST:

Partnerships for impact

Plant scientist Salim Al-Babili and his team, with support from the Bill & Melinda Gates Foundation, are working to eradicate Striga infestation of pearl millet in sub-Saharan Africa. Their technology outsmarts this beautiful but deadly weed by inducing “suicidal germination,” causing the plant to germinate in the absence of the crop it needs to thrive.

Go to discovery.kaust.edu.sa to learn more.

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