A Necrotizing Toxin Promotes Pseudomonas syringae Infection Across Evolutionarily Divergent Plant Lineages

Abstract

The Pseudomonas syringae species complex harbors a diverse range of plant pathogenic bacteria. While much of the current understanding of P. syringae is 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 how P. syringae infects distantly related plants. We identify broad host P. syringae isolates causing significant disease in the liverwort Marchantia polymorpha, the fern Ceratopteris richardii, and the flowering plant Nicotiana 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 the P. syringae species 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 infect Marchantia thalli exhibit enhanced bacterial growth when supplemented with exogenous syringomycin, further highlighting its role as a host-range defining factor in Pseudomonas. Collectively our research reveals a key role for the lipopeptide syringomycin in promoting Pseudomonas colonization, which works in concert with type-3 effector proteins to antagonize an exceptionally wide spectrum of land plants.