Uncovering genetic linkages in the rhizosphere contributing to adaptation

Authors: WILLIAMS, JESSICA - Montana State University; KILLIAN, ERIK - Montana State University; HALPIN-MCCORMICK, ANNA - University Of Hawaii; KANTAR, MICHAEL - University Of Hawaii; SHERMAN, JAMIE - Montana State University; Neupane, Dhurba; EBERLY, JED - Montana State University; LACHOWIEC, JENNIFER - Montana State University

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 11/25/2024
Publication Date: 11/25/2024
Citation: Williams, J.L., Killian, E.Z., Halpin-Mccormick, A., Kantar, M.B., Sherman, J.D., Ewing, P.M., Eberly, J.O., Lachowiec, J. 2024. Uncovering genetic linkages in the rhizosphere contributing to adaptation. bioRxiv. https://doi.org/10.1101/2024.11.21.624704.
DOI: https://doi.org/10.1101/2024.11.21.624704

Interpretive Summary: Microbes that associate with crop roots via the rhizosphere can improve crop performance. Both crop genetics and the local environment control these crop-microbe associations, but these associations are otherwise very poorly understood. Yet-unknown is which genes control these associations with which microbes in which environmental contexts. We fill these gaps using 232 contemporary malting barley lines from US breeding programs, the S2MET population. We grew them in three adapted locations, west and central Montana and eastern South Dakota, plus a new location, Hawaii, over two years, measuring both bacteria in barley’s rhizosphere and barley performance. We also conducted a greenhouse experiment exposing broadly-adapted and local specialist lines from the S2MET population to a combination of soils and microbial inoculants from the Montana locations. We found barley associated with different microbes depending on both the background microbial population and the soil type. These associations were invariably dependent on genetic-by-environment interactions controlling both microbial interactions and plant traits, such as duration of grain fill, that allowed specific barley genotypes to perform better in local conditions. The genetic loci behind these microbial and plant phenotypic traits tended to co-localize and also corresponded with known genes that alter root functions. These findings support the idea that genetic manipulation of rhizosphere microbiomes via selection of crops could enhance adaptation (i.e., yield, quality) across variable environments, advancing breeding strategies for improved crop resilience and productivity.

Technical Abstract: Microorganisms assembled into the p¬lant rhizosphere from the surrounding soil can benefit the fitness of their host. Variation in plant genetics is associated with variation in rhizosphere microbial community composition leading to increased fitness and crop production and reducing reliance on synthetic agricultural inputs through selection. However, what impact the abiotic environment has on connections between microbes and host genetics, and whether those connections in turn impact crop performance in realistic agricultural scenarios is still unclear. We assessed agronomic performance and 16S sequence-based rhizosphere bacterial community composition on a large diverse barley population grown in seven field trials across four locations and two years. Within adapted regions, we observed consistent rhizosphere compositions across diverse soils, whereas unadapted environments recruited distinct microbial communities, indicating environmental specificity in microbial assembly. Greenhouse trials further revealed that abiotic soil properties and microbial inoculants together interact to modulate rhizosphere composition and plant growth. Genome-wide association studies identified hundreds of quantitative trait loci (QTL) for microbial traits, with thirty of those loci co-localizing with agronomic traits, suggesting interspecies pleiotropy or genetic linkage. At specific loci, candidate genes associated with root-microbe interactions, including those related to pathogen response and root exudate production, suggest mechanisms that enable adaptation to local environments. These findings support the idea that genetic manipulation of rhizosphere microbiomes via selection of crops could enhance adaptation (i.e., yield, quality) across variable environments, advancing breeding strategies for improved crop resilience and productivity.