Evolution of drought and desiccation tolerance in grasses

Grasses form the basis of our food system and are important ecologically as the dominant vegetation across wide swaths of land. The abiotic environment has influenced the evolutionary history of this amazing plant family. In particular, water availability is a challenge that has driven adaptation in grasses. Lack of water is also a major challenge for agriculture, both at present and forecasted to become more important in the coming decades. The research in this dissertation explores evolutionary adaptations of grasses to water stress using a comparative genomics framework. In each chapter of this dissertation we compare grass species, or groups of grass species, that differ in their water stress adaptations. Our goal is to identify genetic signatures that enable drought tolerance. We also look for shared responses that give us insight into the essential aspects of drought response that are conserved among diverse grasses. The four chapters in this dissertation look at three comparative systems. (1) We broadly compare two subfamilies of grasses: the Chloridoideae, which are a hub of plant resilience and contain a number of under-resourced crops, and the Panicoideae, which contain some of the world's most important crops but lack the resilience of the Chloridoideae. (2) We compare the desiccation tolerant extremophyte Eragrostis nindensis with its desiccation sensitive cereal crop relative E. tef. (3) We compare sorghum, a crop heralded for its drought resistance, with its more mesic cousin maize. Finally, in chapter four we return to the comparison of E. nindensis and E. tef but we add a new element of time as we look at desiccation tolerance through the lens of a high resolution timecourse.In our first system we conducted a literature review of the physiological, anatomical, and biochemical adaptations of grasses in the Chloridoideae and Panicoideae subfamilies. We focused on crop species within the two families with a focus on many under-resourced cereals. We put forward the hypothesis that panicoid and particularly chloridoid grasses which evolved in dry environments may hold the key to improving the resilience of major crops from more mesic environments. In our second system we looked at the origins of desiccation tolerance in grasses. A leading hypothesis suggests that the same genes which allow many seeds to survive dry conditions could help desiccation tolerant plants during extreme drought. We sequenced the genome of the desiccation tolerant grass E. nindensis and we compared how genes which are normally expressed in seeds behave in leaves during severe water stress in both E. nindensis and E. tef. We found that seed related genes are active in both species during severe stress. In our third system we used a novel machine learning approach to identify shared drought responses in the drought resistant crop sorghum and the more drought susceptible but related crop maize. Our approach found a core set of genes whose expression could predict whether a plant was drought stressed across species. These results suggest that elements of the drought response in grasses are more conserved than previously thought. Finally, we returned to our Eragrostis system but used a much higher resolution timecourse to see how gene expression changed over time. We found that E. nindensis shut down most of its metabolism during dehydration and genes which normally follow a 24 hour cycle of expression stopped cycling. These dramatic changes suggest that E. nindensis uses a pre-programmed orderly shutdown to survive desiccation.