Downy mildew disease-suppressive soils transmit a protective core microbiome to the phyllosphere

Plants can respond to pathogen attack by assembling disease-suppressive soil microbiomes. In Arabidopsis thaliana, infection by the obligate foliar downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) consistently led to the formation of a soil microbial community, termed the soilborne legacy (SBL), that enhanced resistance in subsequent plant populations grown in the same soil. Previous work identified an enrichment of specific Hpa-associated microbiota (HAM) in the phyllospheres of infected plants, which suppressed pathogen proliferation. However, the relationship between rhizosphere and phyllosphere microbiota in generating the SBL and assembling protective HAM remained unclear. Here, we identified a community of 25 core-HAM that consistently dominated the phyllospheres of 14 sets of distinct Hpa-infected plant populations across six independent experiments. Using HAM-free, gnotobiotic Hpa spores, the infection-driven assembly of the core-HAM member Sphingobium ASV ed6be was recapitulated, showing de novo and progressive accumulation under sustained disease pressure. Although HAM transmission in SBL occurred via soil, these bacteria were shown to be phyllosphere specialists, accumulating more abundantly on aboveground than belowground tissues. Moreover, leaf wash-offs from plant populations that inherited SBL, effectively suppressed downy mildew disease when applied to leaves of plants grown in unconditioned soil. These findings reveal that downy mildew disease-suppressive soils transmit a protective core microbiome to the phyllosphere, highlighting a crucial link between belowground and aboveground plant-driven microbiome assembly processes. Paradoxically, the phyllosphere thus emerges as a central hub for the accumulation of disease-suppressive soil microbiomes.

植物可通过组装抑病性土壤微生物组来响应病原菌侵染。在拟南芥（Arabidopsis thaliana）中，专性叶面霜霉病原菌寄生霜霉菌（Hyaloperonospora arabidopsidis，Hpa）的侵染会持续形成一类被称为土壤遗留微生物组（soilborne legacy，SBL）的土壤微生物群落，该群落可增强后续在同一土壤中生长的植物种群的抗病性。既往研究已发现，侵染植株的叶圈（phyllosphere）中会富集一类特定的Hpa相关微生物组（HAM），该类微生物组可抑制病原菌增殖。然而，根际（rhizosphere）与叶圈微生物组在构建SBL以及组装保护性HAM过程中的关联仍未明确。
本研究通过6组独立实验，在14组不同的Hpa侵染植物种群的叶圈中，鉴定出了由25个核心HAM（core-HAM）组成的群落，该群落始终占据叶圈微生物组的主导地位。我们使用无HAM的无菌培养（gnotobiotic）Hpa孢子，重现了侵染驱动的核心HAM成员鞘氨醇单胞菌（Sphingobium）扩增子序列变异体（Amplicon Sequence Variant，ASV）ed6be的组装过程，观察到其在持续病害压力下从头起始并逐步积累。尽管SBL中的HAM可通过土壤进行传播，但这类细菌被证实为叶圈专性菌，在地上组织中的丰度显著高于地下组织。此外，从携带SBL的植物种群中获取的叶片洗脱液，施加到在未预处理土壤中生长的植株叶片上时，可有效抑制霜霉病的发生。
本研究结果表明，抑病性霜霉病土壤可向叶圈传递具有保护作用的核心微生物组，凸显了地下与地上植物驱动的微生物组组装过程之间的关键关联。颇具矛盾的是，叶圈就此成为抑病性土壤微生物组积累的核心枢纽。