Fabrice Roux, Laboratoire des Interactions Plantes-Microbes-Environnement, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, CNRS, Université de Toulouse, Castanet-Tolosan, France.
Department of Systematic and Evolutionary Botany, University of Zurich, Zürich, Switzerland.
Mol Biol Evol. 2023 May 2;40(5). doi: 10.1093/molbev/msad093.
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-environment 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 nonmicrobial 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 nonmicrobial ecological factors. Importantly, the relative importance of host genetics and nonmicrobial ecological factors in explaining the presence of particular operational taxonomic units (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 quantitative trait loci (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.
了解宿主基因组在调节微生物群落变异中的作用，是阐明整体生物理论和克服当前在基因组和分子水平上描述宿主-微生物相互作用的局限性的需要。然而，在植物中，只有部分描述了宿主遗传结构对微生物群落的结构作用。此外，大多数关于微生物组的关联遗传研究通常是在宿主进化的自然栖息地之外进行的，而对候选基因上的本地适应特征的鉴定被忽视了。为了填补这些空白并剖析驱动适应性植物-微生物相互作用的遗传结构，我们对 141 个全基因组测序的拟南芥自然种群进行了全基因组-环境关联（GEA）分析，这些种群在秋季和春季原位表征了它们的叶片和根部细菌群落，以及广泛的非微生物生态因子（即气候、土壤和植物群落）。与非微生物生态因子相比，宿主遗传学解释了种群间微生物群落差异的更大比例。重要的是，宿主遗传学和非微生物生态因子在解释特定操作分类单元（OTU）存在方面的相对重要性因细菌科和属而异。此外，对细菌群落的适应的多基因结构在植物隔室和季节之间具有高度的灵活性。相关地，在春季，根系微生物组的数量性状基因座（QTL）上具有更强的本地适应特征。最后，植物免疫似乎是拟南芥中细菌组合结构的适应性遗传变异的主要来源。
