Unlocking cellular decision making for plant plasticity and crop sustainability
Alexander Jones, Head of Jones Group, Sainsbury Laboratory Cambridge University
Plants are rooted beings lacking sensory organs and centralised information processing, yet they thrive in dynamic and challenging environments. Precisely how they do this is not just a fascinating question of genetically programmed flexibility, but also an urgent question of agri-food sustainability with climate change pushing crop plasticity to uncharted territory. For example, rice - the world’s number one food crop - is predicted to have up to 25% yield losses with just 1 degree of warming. Much of the answer lies in the dynamics of plant hormones, a chemically diverse set of mobile molecules that process information by integrating environmental and internal cues followed by activating plastic traits like drought tolerance or immunity. For example, the plant hormone auxin responds dynamically to environmental cues like light, temperature, nutrients and signals from symbionts, pathogens and pests while shaping growth, morphology, developmental transitions and stress responses. This potency, where individual hormones regulate so many processes, presents an enduring mystery as to how information is decoded and encoded with specificity. High potency also means hormones are prime targets for engineering novel plasticity, provided we can achieve sufficiently precise understanding and targeting.
Visualising cellular hormone dynamics to reveal the role of plant hormones in governing plant development and physiology.
Tiny amounts of these small, mobile chemicals can reprogramme a plant cell and completely change its growth and physiology. Which plant cells produce these chemicals? Where and when do these chemical hormones go? Precisely what are these chemicals doing when they get there? These are the core questions about plant hormones that my group is trying to answer. With this information, we aim to discover high-leverage hormone targets for engineering crops that are more sustainable with minimal off-target effects. This means helping plants be resilient to environmental stresses like flash floods and flash droughts and helping them to thrive with less inputs and using less land.
Why Cambridge?
The University of Cambridge is home to one of the largest concentrations of plant research anywhere in the world and has a long history of ground-breaking plant hormone research. For example, current Regius Professor of Botany Dame Ottoline Leyser’s seminal contributions to auxin and strigolactone signal transduction and hormone mediated plant development, and Darwin and Darwin (1880) contributing some of the very first observations of hormone activity in plants.
Why now?
Cellular hormone dynamics. Biology is engaged in a single-cell revolution motivated by the emergence of function from ensemble cellular decision making and enabled by novel technologies permitting study of single cell types, or even individual cells in a living organism. This is particularly true in plants that have few organ systems and no unique parts. But how to quantify mobile hormone dynamics given their low-concentrations, small size, rapid changes, and (sub)cellular patterns? My group has pioneered the solution by engineering high-resolution, genetically-encoded biosensors for four plant hormones that regulate growth, development, drought response and immunity (i.e. Fluorescence Resonance Energy Transfer (FRET) biosensors). Using these fluorescent tools, we have revealed, for the first time, single-cell hormone dynamics in living plants, how they are ‘encoded’ and their quantitative functions once they are ‘decoded’ (Fig. 1). Early on, we saw a critical limitation of the broader single-cell revolution in plants – to test high-resolution biological hypotheses (e.g. from our fluorescent biosensing), we need resolved perturbation. So we engineered Highlighter, an optically controlled gene expression switch for plants that allows us to turn genes on and off in neighbouring cells. Our initial aims for plant optogenetics were in fundamental research, but we also aim to engineer tools for on-demand plasticity in crops. For example, using light to re-direct genes regulating plant hormones to adjust the plant’s immune system ahead of a disease outbreak, or conserve water before an extreme weather event.
Any outputs, outcomes or impact that is measurable. Has this or can it translate to clinical, society or industry uses?
Using the genetical model organism Arabidopsis thaliana, my group dug deep into how roots and shoots pattern the growth hormone GA into a gradient with high levels in the longest cells (e.g. Fig. 1), how these patterns relate to cell growth (not a simple dose-response dynamic) and collaborated with mathematicians to overturn and replace earlier chemical-cellular-organ models of how hormones are arranged in living plants.
Using biosensors for the ‘water stress hormone’ ABA, we found novel cellular ABA dynamics coordinating root growth with leaf humidity stress in Arabidopsis, with potential implications for irrigation agriculture under climate change. For example, through a combined in vivo biochemistry, mathematical modelling and precision genetics approach, we aim to discover and then engineer ABA hormone redistribution to help irrigated plants face hot and dry air in increasingly severe and prevalent ‘flash droughts’.
As a first step to impact for society, we have deployed our biosensors to reveal GA and ABA dynamics in diverse species including crops like rice and wheat, bringing us closer to understanding the cellular decision making controlled by hormones in important crop traits. In a legume closely related to pea that recruits a soil bacterium for nitrogen-fixing symbiosis, we and the Oldroyd group in the Crop Science Centre collaborated to resolve a spatiotemporally defined role for GA in promoting symbiotic organ formation, adding cell-level clarity to low-resolution studies indicating both activation and repression by GA. We confirmed function for this local GA accumulation using precision genetics and these insights can now guide strategies to boost symbiosis, potentially reducing fertilizer use and increasing legume crop yields through targeting GA increases to the right cells at the right time.
What are the milestones, timelines and what happens next?
Despite enormous progress in hormone biochemistry and signalling, how coherent and appropriate responses to environmental stimuli arise from hormone dynamics remains enigmatic. Low-resolution hormone measurements and genetics have yielded enormous insight into components that influence hormone dynamics during plant plasticity. Yet knowing the instruments does not reveal the concerto. We aim to use cellular biosensing and optogenetics to reveal fundamental rules of information encoding and decoding via hormones, and, with time, to use these insights to helping plants repattern hormones to cope with realistic environmental conditions, particularly current and future climate stresses. We imagine a more distant future where on-demand plasticity will enable growers to repattern hormones to optimise growth and developmental transitions or help plants prepare for oncoming drought and pathogen outbreaks.
If we solve the problem what can we expect
With cellular measurements and high-resolution genetics, we hope to help deliver the multiscale deconvolution needed to fully grasp how hormones enable multicellular life to thrive in complex environments, and to help others use this information to engineer hormone-based solutions for agricultural sustainability.