A plant genetic network for preventing dysbiosis in the phyllosphere

The aboveground parts of terrestrial plants (collectively called phyllosphere) are sometimes considered to be the “lungs of the planet” and represent one of the most abundant habitats for microbiota colonization on earth. Whether and how plants control phyllosphere microbiota to ensure plant health is poorly understood. Here we show that the Arabidopsis quadruple mutant (min7 fls2 erf cerk1; mfec(1) hereinafter) simultaneously defective in pattern-triggered immunity and the MIN7 vesicle traffic pathway or the constitutively activated cell death1 (cad1) mutant defective in a “membrane-attack-complex/perforin (MACPF) domain” protein have altered endophytic phyllosphere microbiota and display leaf tissue damages associated with dysbiosis. The relative abundance of Firmicutes was dramatically reduced, whereas Proteobacteria were enriched in the mfec and cad1 mutants, bearing some cross-kingdom resemblance to what occurs in human inflammatory bowel disease. Bacterial community transplantation experiments demonstrated a causal role of a properly assembled leaf bacterial community in phyllosphere health. Pattern-triggered immune signaling, MIN7 and CAD1 are found in major land plant lineages and are likely key components of a genetic network through which terrestrial plants control the level and nurture the diversity of endophytic phyllosphere microbiota for survival and health in a microbe-rich environment.