Using Performance-Based Insights into the Sorghum Microbiome to Advance Microbiome-Mediated Solutions in Arid Agriculture

Abstract

Increasingly, the crop microbiome is looked to as a novel toolkit to combat abiotic stressors while sustaining agricultural productivity, essential to overcoming ecological challenges associated with agricultural intensification in a changing world. Despite recent advances in characterizing species that comprise plant microbiomes, specific ways by which a given microbiome contributes to crop performance remains unclear. Broadly defined, the endophytic microbiome consists of microbes that inhabit the interior of plant tissues without causing symptoms of disease. As such, endophytes in that establish in roots and leaves form intimate relationships with their plant host, at times existing as commensals but in other cases altering plant phenotypes. Because endophytes have a long evolutionary history with plants, they depend on plants complete their life cycle, and they either evade or overcome plant defenses to establish, it is thought that many can be beneficial for plant growth and resilience to stress. However, knowledge gaps remain a challenge for applications of endophytes: how do they vary among genotypes of plants? What are their growth-influencing traits? Do potentially beneficial endophytes harbor genes associated with production of undesirable secondary metabolites? How can endophytes be selected and delivered to plants effectively for improvements in agriculture? This dissertation centers on characterizing the fungal and bacterial endophytic microbiome of sorghum, a stress-resilient cereal crop, and developing a pipeline for selection of beneficial root-associated bacteria for plant growth and yield promotion. Together with my coauthors, I show that the sorghum root microbiome shifts under drought, and that the microbiome of higher-performing lines may be especially responsive to drought. However, drought does not remodel microbe-microbe interactions, suggesting that host-microbe interactions underlie microbiome shifts under environmental stress. To test this prediction, I, with my colleagues, analyzed the root metabolome and interpreted its relationship to specific microbial taxa. Relative to lower-performing lines, higher-performing sorghum accumulated a lower level of flavonoids, which are members of a phytohormone class strongly linked to defense and may facilitate establishment of root-endophytic microbes with plant-growth promoting potential. To understand the genomic architecture of representative root-associated bacteria, my colleagues and I used whole-genome sequencing to explore secondary metabolite production and other genomic features of microbes associated with high-performing sorghum from field conditions in Arizona. Finally, we evaluated a biobank of sorghum cultures, testing the prediction that those associated with higher-performing plants would be more likely to show plant growth-promoting phenotypes in vitro, including phosphate solubilization, auxin production, ammonium production, and siderophore activity. Based on bioassay results, a suite of microbial strains was used in a greenhouse and field experiment to evaluate the potential of microbial inoculants to promote desirable phenotypes in sorghum. We found that microbial inoculants associated with plant growth promotion were successful at promoting biomass and yield in a field-grown sorghum hybrid line, with differences relative to greenhouse results suggesting a strong impact of field-relevant stressors or other conditions. Overall, this work strengthens our understanding of how plant microbiomes relate to plant phenotypes, and provides a framework for a translatable approach to manipulate microbes for field applications.