Genetic determinants of switchgrass-root-associated microbiota in field sites spanning its natural range

• Published in: Current biology 2023-05, Vol.33 (10), p.1926-1938.e6
• Main Authors: Edwards, Joseph A., Saran, Usha Bishnoi, Bonnette, Jason, MacQueen, Alice, Yin, Jun, Nguyen, Tu uyen, Schmutz, Jeremy, Grimwood, Jane, Pennacchio, Len A., Daum, Chris, Glavina del Rio, Tijana, Fritschi, Felix B., Lowry, David B., Juenger, Thomas E.
• Format: Article
• Language: English
• Subjects: Bacteria - genetics; BASIC BIOLOGICAL SCIENCES; biofuel feedstocks; ENVIRONMENTAL SCIENCES; Genome-Wide Association Study; Genotype; GWAS; heritability; immunity; microbiome; Microbiota; Panicum - genetics; pattern-triggered immunity; plant microbiome; switchgrass
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2023.03.078

A fundamental goal in plant microbiome research is to determine the relative impacts of host and environmental effects on root microbiota composition, particularly how host genotype impacts bacterial community composition. Most studies characterizing the effect of plant genotype on root microbiota undersample host genetic diversity and grow plants outside of their native ranges, making the associations between host and microbes difficult to interpret. Here, we characterized the root microbiota of a large diversity panel of switchgrass, a North American native C4 bioenergy crop, in three field locations spanning its native range. Our data, composed of 1,961 samples, suggest that field location is the primary determinant of microbiome composition; however, substantial heritable variation is widespread across bacterial taxa, especially those in the Sphingomonadaceae family. Despite diverse compositions, relatively few highly prevalent taxa make up the majority of the switchgrass root microbiota, a large fraction of which is shared across sites. Local genotypes preferentially recruit/filter for local microbes, supporting the idea of affinity between local plants and their microbiota. Using genome-wide association, we identified loci impacting the abundance of >400 microbial strains and found an enrichment of genes involved in immune responses, signaling pathways, and secondary metabolism. We found loci associated with over half of the core microbiota (i.e., microbes in >80% of samples), regardless of field location. Finally, we show a genetic relationship between a basal plant immunity pathway and relative abundances of root microbiota. This study brings us closer to harnessing and manipulating beneficial microbial associations via host genetics. •A large proportion of root-associated bacteria show heritable variation•Genotypes growing in their native habitat show affinity to the local microbiota•Microbiome acquisition is a genetically complex trait varying by environment•Root microbiome variation correlates with variation in host immunity phenotypes Plant roots are a hotspot for colonization by soil bacteria that can greatly impact host fitness. Edwards et al. investigate the role of host plant genotype in determining the composition of root microbiota in switchgrass, a North American native perennial species. They find a large proportion of the root microbiota is under host genetic control.