CAREER: Rapid evolution of an invasive plant: the role of microbial interactions

It is now clear that microbiomes can have large impacts on the health and performance of organisms. Microbiomes include thousands of microbe species, however, and what is not clear is how multicellular organisms have evolved to optimize their interactions with this complex microbial community, particularly in terms of optimizing immune defenses against many different microbial diseases at once. In plants, there is a fundamental trade-off between investments in defense and growth, and optimizing defense activity is essential to maximizing growth and fitness in a microbial environment. Plant species that have been introduced by humans to different regions of the globe offer especially good opportunities to test hypotheses about how plants can optimize their responses to natural differences in microbial communities. The European plant yellow starthistle (Centaurea solstitialis) is highly invasive in grasslands of the Americas, where it enjoys more favorable interactions with soil microbes and it has evolved increased growth and reproductive ability. This project will identify the microbes involved in these interactions and the mechanisms by which the invading plant populations have evolved to increase their growth under different microbial environments. The research will contribute novel advancements in the understanding of interactions between organisms and their microbiomes, with specific opportunities for improved management of agricultural systems. An important component of the project is the creation of an undergraduate research community focused on improving the confidence and retention of disadvantaged students who desire to complete a degree in biology and promoting the retention of high-achieving students with training in plant-microbial interactions.<br/><br/>In its severe invasion of the western US, yellow starthistle experiences more favorable microbial interactions with the soil, and the principal investigator has recently identified i) reduced diversity of bacteria and ii) an apparent reduction in plant investment in aspects of immune function in these populations. The principal investigator has also identified candidate regions of the genome associated with these rapid evolutionary changes. This project will identify key microbial taxa involved in these interactions and their effect on plant evolution through 1) sequencing of the microbiome across multiple generations of plant-soil feedback experiments, 2) selection experiments with the microbial community to identify the impacts of microbial evolution on plant traits, 3) selection on plant genotypes to identify the genetic basis of fitness differences and to quantify trait evolution under different microbial environments, and 4) gene expression studies to identify plastic and genetic responses of pathways to microbial interactions. Undergraduate students from groups underrepresented in STEM will lead studies of individual microbial taxa in culture and their effects on plant immune responses. The proposed research will be among the first to characterize the microbial community responsible for natural variation in microbial interactions and feedbacks with plant genotypes, to identify the plant loci involved in plastic and evolutionary response to this community variation, and to test alternative hypotheses regarding how microbiome variation can contribute to evolution along growth-defense trade-offs. These contributions will fundamentally advance understanding of the nature of selection on growth and defense generated by interactions with a complex microbial community.<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.