CAREER: Drivers of Plant-Microbe Symbiosis Evolution During Crop Domestication

Over thousands of years of domestication and crop improvement, humans have shaped hundreds of wild plant species into the diverse crops we depend upon. While beneficial microbes that live on and inside of plants play key roles in plant health, little is known about how a plants? ability to benefit from these cooperative microbes changes during domestication. Plant-microbe cooperation is not stable. In fact, plants have repeatedly abandoned cooperation with microbes over evolutionary time, and growing evidence shows that some crops evolve to depend less on microbes over the course of domestication. This reveals a gap in our understanding of the evolution of cooperation: what evolutionary processes result in abandoning cooperation? And why does cooperation with microbes decline for some plant species, but not others? To investigate how these symbiotic relationships differ between modern crops and their wild relatives, this project will use seed collections and genomic resources for legume crops ranging from soybeans to peas. The utility of legumes in agriculture lies in their unique symbiosis with rhizobial bacteria, which convert atmospheric nitrogen into chemical forms usable to plants, essentially fertilizing them. At least forty-one legume species have been domesticated. Researchers will compare domesticated legumes? ability to benefit from rhizobia to that of their wild relatives by using modern genetic and analytical approaches. These techniques will provide insight into how natural selection has changed patterns of cooperation between legumes and rhizobia during domestication. Legumes account for a quarter of global crop production and a third of human dietary protein. Understanding how and why rhizobial symbiosis has evolved during domestication will provide a critical road map for ways in which we could improve crop yield in order to increase our ability to feed our growing human population. Crop domestication is also a tangible example of evolution in action--domesticated species have provided an intuitive model for evolutionary biology since Darwin?s original arguments. Project research will engage undergraduates with evolutionary problems in familiar food crops. To increase the inclusion of underrepresented minority and community college transfer students in science, the researchers will develop a new Course-based Undergraduate Research Experience (CURE) module on symbiosis and crop domestication and a new Science Scholars Program to recruit and retain diverse undergraduates in scientific research.<br/><br/>A paradigm shift in the field of mutualism evolution is a newfound appreciation for the frequency with which host organisms, such as plants, have abandoned mutualisms with symbiotic microbiota. Yet, little is known about the micro-evolutionary processes that lead to declines in host symbiosis traits. This project will use germplasm and genomic resources that exist for legume crops as a powerful system with which to investigate declines in plant symbiosis traits over replicated evolutionary lineages from wild plants to modern elite cultivars. By integrating approaches from phylogenetics, molecular genetics, quantitative genetics, and genomics, this project will contribute fundamental knowledge about the role of trade-offs, natural selection, and genetic costs in shaping micro-evolutionary dynamics in symbiotic mutualism. To elucidate the traits, forms of selection, and loci that underlie changes in legume-rhizobium symbiosis across thousands of years of evolution in agriculture, researchers will: 1) quantify how the nitrogen-fixing symbiosis with rhizobia differs between leguminous crops and their wild relatives, 2) test whether legume symbiosis traits have negative genetic correlations with legume traits favored under artificial selection, 3) test whether fertilization relaxes selection on legume symbiosis traits or selects for reduced symbiosis, and 4) infer whether genetic costs of domestication are predicted to degrade symbiosis traits in crops. This work will pave the way towards integrating an understanding of the evolutionary forces and constraints that underlie dynamics between hosts and microbial symbionts into the mainstream of evolutionary biology.<br/><br/>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.