The Genetic Architecture of Adaptation to Leaf and Root Bacterial Microbiota inArabidopsis thaliana

Abstract

Understanding the role of the host genome in modulating microbiota variation is a need to shed light on the holobiont theory and overcome the current limits on the description of host-microbiota interactions at the genomic and molecular levels. However, the host genetic architecture structuring microbiota is only partly described in plants. In addition, most association genetic studies on microbiota are often carried out outside the native habitats where the host evolves and the identification of signatures of local adaptation on the candidate genes has been overlooked. To fill these gaps and dissect the genetic architecture driving adaptive plant-microbiota interactions, we adopted a Genome-Environmental-Association (GEA) analysis on 141 whole-genome sequenced natural populations of Arabidopsis thaliana characterized in situ for their leaf and root bacterial communities in fall and spring, and a large range of non-microbial ecological factors (i.e. climate, soil and plant communities). A much higher fraction of among-population microbiota variance was explained by the host genetics than by non-microbial ecological factors. Importantly, the relative importance of host genetics and non-microbial ecological factors in explaining the presence of particular OTUs differs between bacterial families and genera. In addition, the polygenic architecture of adaptation to bacterial communities was highly flexible between plant compartments and seasons. Relatedly, signatures of local adaptation were stronger on QTLs of the root microbiota in spring. Finally, plant immunity appears as a major source of adaptive genetic variation structuring bacterial assemblages in A. thaliana.

Biotic interactions promote local adaptation to soil in plants

“…Local adaptation is mediated by many features of the environment, because selection in natural habitats is usually driven by a set of interacting factors, including abiotic and biotic ones 28,43 . Nevertheless, the traditional research focus in local adaptation has been on abiotic factors such as climate, or mixed abiotic-biotic factors such as soil 29 , even though biotic factors such as herbivores, pollinators, microbiota, or competitors are equally or sometimes even more important than abiotic factors for plant survival and reproduction 28,44–47 . How quickly organisms adapt to the multivariate local habitat conditions 15,35 , and which genomic changes enable such adaptation 17 is not well known, despite the importance of rapid adaptation to the survival of many organisms in the face of regional- and global change.…”

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

“…However, studies of holobionts in their native habitats are still underrepresented. To our knowledge, Roux et al, 2023 is the only large plant in situ survey describing a highly variable genetic architecture between plant compartments (leaves and roots) and seasons (fall and spring) for the bacterial A. thaliana microbiome (12). As mentioned by the authors, the next step is to compare fungal and bacterial microbiomes in situ to identify common plant genetic loci structuring inter-kingdom interactions.…”

“…Recently, studies showed the power of GEA to identify plant loci associated with biotic communities. This has been demonstrated both in the non-model plant species B. incana and its associated pollinator communities (10), and in the model plant species Arabidopsis thaliana and its plant-plant (11) and plant-microbiome (12) interactions. The latter study is the only describing adaptive loci associated with bacterial descriptors in natural plant populations.…”

“…GEA analysis was performed on microbiota descriptors (species richness, Shannon's diversity, PCoA first four axes and abundance of the most prevalent fungal and bacterial OTUs) as described in Roux et al, 2023 andFrachon et al, 2023 (10, 12). Detailed information about GEA analysis and related scripts are provided in the SI Appendix.…”

Rhizosphere Microorganisms Supply Availability of Soil Nutrients and Induce Plant Defense

“…The impact of the microbiome on plant health, particularly in the context of Arabidopsis thaliana , a model organism for plant biology, has been extensively studied and reveals complex interactions [ 174 , 175 , 176 , 177 ]. These studies have shown that healthy plants host diverse and structured communities of microorganisms that colonize almost every part of the plant [ 177 , 178 , 179 ]. This plant-associated microbiome offers significant advantages to the host, including promoting growth, aiding in nutrient uptake, enhancing stress tolerance, and providing resistance to pathogens [ 180 ].…”