Collaborative Research: RESEARCH-PGR: Unraveling the origin of vegetative desiccation tolerance in vascular plants

Climate change is increasing the frequency and severity of drought events around the world, leading to major losses in crop productivity, which affect future food security. Consequently, the generation of crops with enhanced drought tolerance represents an urgent need for breeders, scientists, and governments. Excessive water loss is lethal for most plants, but a few plants, known as resurrection plants, have the remarkable ability to survive almost complete dehydration of their green tissues. This ability, known as vegetative desiccation tolerance (VDT), relies upon a combination of molecular processes that allow the plant to maintain its viability in the dry state. Interestingly, all genes involved in VDT are also present in desiccation-susceptible plants, as most plants produce seeds that can survive for long periods in the dry state without losing the capacity to germinate upon watering. Therefore, the difference between tolerant and susceptible plants must be in their capacity to activate the mechanisms that protect cells against desiccation in green tissues and not only in the seed. The objective of this project is to identify the mechanisms of how plants evolved to activate desiccation tolerance in both vegetative and reproductive tissues. Specifically, this study seeks to identify the genes that act as master regulators of desiccation tolerance. This collaborative project will use a multidisciplinary approach to identify common and specific molecular processes by comparing the dynamic responses of green tissues and seeds. The results of this project will serve to design molecular breeding schemes for improving crop resilience to climate change. Excessive water loss is lethal for most plants, but a few species, known as resurrection plants, evolved the remarkable ability to survive almost complete dryness. This ability, known as desiccation tolerance (DT), relies upon a combination of physiological, biochemical, and molecular responses that allow the plant to preserve cell integrity in the dry state. Interestingly, all gene families involved in vegetative desiccation tolerance (VDT) are present in desiccation-sensitive plants, suggesting that this trait evolved primarily by changes in the regulatory networks coordinating the expression of DT genes rather than from the acquisition of new genes. The lack of accurate comparative analyses has hindered the identification of the regulators controlling VDT and the study of the evolutionary origin of this trait in vascular plants. Therefore, this collaborative project will determine the regulatory networks controlling VDT and infer its origin during vascular plant evolution by analyzing the DT response of key resurrection lineages using integrative methodologies. Specific objectives include (1) determining the kinetics of the global transcriptional changes in vegetative and reproductive tissues during the DT process, (2) performing kinetic analyses of the global metabolic changes in vegetative and reproductive tissues during the DT process, (3) performing in situ and single-cell type kinetic analysis of transcriptional and metabolomic changes of vegetative tissues during dehydration and recovery, and (4) conducting comparative analyses of the regulatory networks controlling DT in resurrection plants. This study will identify genetic-metabolic networks required to activate VDT, providing the basis for future crop breeding of enhanced drought tolerance. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.