A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota

The identity of plant host genetic factors controlling the composition of the plant microbiota and the extent to which plant genes affect associated microbial populations is currently unknown. Here, we use a candidate gene approach to investigate host effects on the phyllosphere community composition and abundance. To reduce the environmental factors that might mask genetic factors, the model plant Arabidopsis thaliana was used in a gnotobiotic system and inoculated with a reduced complexity synthetic bacterial community composed of seven strains representing the most abundant phyla in the phyllosphere. From a panel of 55 plant mutants with alterations in the surface structure, cell wall, defense signaling, secondary metabolism, and pathogen recognition, a small number of single host mutations displayed an altered microbiota composition and/or abundance. Host alleles that resulted in the strongest perturbation of the microbiota relative to the wild-type were lacs2 and pec1. These mutants affect cuticle formation and led to changes in community composition and an increased bacterial abundance relative to the wild-type plants, suggesting that different bacteria can benefit from a modified cuticle to different extents. Moreover, we identified ein2, which is involved in ethylene signaling, as a host factor modulating the community's composition. Finally, we found that different Arabidopsis accessions exhibited different communities, indicating that plant host genetic factors shape the associated microbiota, thus harboring significant potential for the identification of novel plant factors affecting the microbiota of the communities.目前，调控植物微生物组（plant microbiota）组成的宿主遗传因子身份，以及植物基因影响相关微生物种群的程度尚未阐明。本研究采用候选基因策略，探究宿主对叶际（phyllosphere）群落组成与丰度的影响。为规避可能掩盖遗传效应的环境因素干扰，本研究利用限菌培养体系（gnotobiotic system）中的模式植物拟南芥（Arabidopsis thaliana），接种由7株代表叶际最丰富菌门的菌株组成的低复杂度合成细菌群落。我们对55株涉及表面结构、细胞壁、防御信号通路、次生代谢以及病原识别功能的植物突变体进行筛选，发现少量单宿主突变可导致微生物组组成和/或丰度发生改变。相较于野生型，对微生物组扰动最强的宿主等位基因为lacs2与pec1。这两个突变体影响角质层（cuticle）形成，相较于野生型植株，其群落组成发生改变且细菌丰度升高，表明不同细菌可在不同程度上从修饰后的角质层中获益。此外，我们鉴定出参与乙烯信号通路的ein2作为调控群落组成的宿主因子。最后，我们发现不同拟南芥生态型（Arabidopsis accessions）拥有不同的叶际群落，这表明植物宿主遗传因子可塑造相关微生物组，因此该研究具备发掘调控群落微生物组的新型植物因子的巨大潜力。