Host genotype, soil composition, and geo-climatic factors shape the fonio seed microbiome

Fonio (Digitaria exilis), an orphan millet crop, is the oldest indigenous crop in West Africa. Although the yield is low due to pre-domestication characteristics, the quick maturation time, drought tolerance, and the ability to thrive on poor soils make fonio a climate-smart crop. Being holobionts, plants evolve in close interaction with microbial partners, which is crucial for plant phenology and fitness. As seeds are the bottleneck of vertically transmitting plant microbiota, we proposed to unravel the seed microbiome of the under-domesticated and resilient crop fonio. Our study investigated the bacterial seed endophyte diversity across 126 sequenced fonio accessions from distinct locations in West Africa. We conducted a correlation study of the structures and functions of the seed-associated microbiomes with the native geo-climate and soil structure data. We also performed Genome-wide association studies (GWAS) to identify genetic loci associated with seed endophyte diversity. We report that fonio millet has diverse heritable seed endophytic taxa. We analyzed the seed microbiomes of 126 fonio accessions and showed that despite the diversity of microbiomes from distinct geographical locations, all fonio genetic groups share a core microbiome. In addition, we observed that native soil composition, geo-climatic factors, and host genotype correlate with the seed microbiomes. GWAS analysis of genetic loci associated with endophyte seed bacterial diversity identified fonio SNPs associated with genes functioning in embryo development and stress/defense response. Analysis of the seed endophyte of the climate-smart crop fonio indicated that despite possessing a heritable core microbiome, native conditions may shape the overall fonio seed microbiomes in different populations. These distinct microbiomes could play important roles in the adaptation of fonio to different environmental conditions. Our study identified the seed microbiome as a potential target for enhancing crop resilience to climate stress in a sustainable way. Video Abstract.