Congruent downy mildew-associated microbiomes reduce plant disease and function as transferable resistobiomes

Abstract

SummaryRoot-associated microbiota can protect plants against severe disease outbreaks. In the model-plantArabidopsis thaliana, leaf infection with the obligate downy mildew pathogenHyaloperonospora arabidopsidis(Hpa) results in a shift in the root exudation profile, therewith promoting the growth of a selective root microbiome that induces a systemic resistance againstHpain the above-ground plant parts. Here we show that, additionally, a conserved subcommunity of the recruited soil microbiota becomes part of a pathogen-associated microbiome in the phyllosphere that is vertically transmitted with the spores of the pathogen to consecutively infected host plants. This subcommunity ofHpa-associated microbiota (HAM) limits pathogen infection and is therefore coined a “resistobiome”. The HAM resistobiome consists of a small number of bacterial species and was first found in our routinely maintained laboratory cultures of independentHpastrains. When co-inoculated withHpaspores, the HAM rapidly dominates the phyllosphere of infected plants, negatively impactingHpaspore formation. Remarkably, isogenic bacterial isolates of the abundantly-present HAM species were also found in strictly separatedHpacultures across Europe, and even in early published genomes of this obligate biotroph. Our results highlight that pathogen-infected plants can recruit protective microbiota via their roots to the shoots where they become part of a pathogen-associated resistobiome that helps the plant to fight pathogen infection. Understanding the mechanisms by which pathogen-associated resistobiomes are formed will enable the development of microbiome-assisted crop varieties that rely less on chemical crop protection.