A Necrotizing Toxin PromotesPseudomonas syringaeInfection Across Evolutionarily Divergent Plant Lineages

Abstract

ABSTRACTThePseudomonas syringaespecies complex harbors a diverse range of plant pathogenic bacteria. While much of the current understanding ofP. syringaeis centered on interactions with flowering plants, much less is known about infection in evolutionarily divergent non-flowering lineages. Here, we took a comparative evolutionary approach to understand howP. syringaeinfects distantly related plants. We identify broad hostP. syringaeisolates causing significant disease in the liverwortMarchantia polymorpha, the fernCeratopteris richardii, and the flowering plantNicotiana benthamiana, which last shared a common ancestor over 500 million years ago. We demonstrate that phytotoxin enriched isolates belonging to the phylogroup 2 clade of theP. syringaespecies complex are particularly virulent in non-flowering plants, relying on a combination of type-3 secreted effector proteins and the lipopeptide phytotoxin syringomycin. The application of purified syringomycin promotes necrosis in diverse host tissues and activates conserved genes associated with redox regulation and cell death. Toxin-deficient phylogroups normally unable to infectMarchantiathalli exhibit enhanced bacterial growth when supplemented with exogenous syringomycin, further highlighting its role as a host-range defining factor inPseudomonas. Collectively our research reveals a key role for the lipopeptide syringomycin in promotingPseudomonascolonization, which works in concert with type-3 effector proteins to antagonize an exceptionally wide spectrum of land plants.