Identifying Plant Genes Shaping Microbiota Composition in the Barley Rhizosphere

Abstract

A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we used metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identified a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS locus, emerged as a major determinant of microbiota composition. We then subjected soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allowed us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide novel insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

“…These GWAS revealed a highly polygenic architecture, suggesting a control of natural microbiota assembly by an extensive number of Quantitative Trait Loci (QTLs) with a small effect. A similar result was recently obtained with traditional linkage mapping performed in barley (Escudero-Martinez et al 2022) and tomato (Oyserman et al 2022).…”

Defining composition and function of the rhizosphere microbiota of barley genotypes exposed to growth-limiting nitrogen supplies

“…Consequently, and despite the limited number, these genotypes may capture the “extremes” of the evolutionary pressure on the host recruitment cues of the barley microbiota. Plants were grown under glasshouse conditions (Methods) in an agricultural soil previously used for microbiota investigations and designated ‘Quarryfield’ (31, 33, 34, 40). Pots containing the individual genotypes, and unplanted soil controls (hereafter ‘Bulk’), were supplemented with three modified Hoagland’s solution preparations (41) containing all essential macro and micronutrients and three levels of mineral nitrogen (Table S1): the optimum required for barley growth (N100%), a quarter of dosage (N25%) or no nitrogen (N0%).…”

“…As wild and domesticated barley plants display differential responses to nitrogen fertilisation (50) and a genotype-dependent control of rhizodeposition (51), the characterisation of primary and secondary metabolites released in the barley rhizosphere may provide mechanistic insights into microbiota diversification in barley. However, as recent investigations revealed that the host genetic control of the rhizosphere microbiota in wild and domesticated barley display a quantitative inheritance (32, 34), additional experiments with dedicated genetic material are required to untangle the molecular mechanisms linking nitrogen availability with microbiota diversification.…”

“…Plant-soil feedback experiments suggest that these distinct compositional and functional configurations of the microbiota can be “rewired” by the host genotype leading to a recruitment of a consortium of bacteria putatively required for optimum plant growth. Thanks to recent insights into barley genes shaping the rhizosphere microbiota (32, 34), these concepts can now be tested under laboratory and field conditions to expedite the development of plant varieties combining profiting from improved yields with reduced impacts of N-fertilisation on the environment.…”

“…spontaneum) barley genotypes host microbiotas of contrasting composition (30,31). More recently, we gathered novel insights into the genetic basis of this host-mediated microbiota diversification (32)(33)(34). In parallel, investigations targeting specific microbial genes indicated that barley plants may exert a control on microbes underpinning the nitrogen biogeochemical cycle (35) and that this effect is dependent on community composition (36).…”