A necrotizing toxin enables Pseudomonas syringae infection across evolutionarily divergent plants

Abstract

The Pseudomonas syringae species complex harbors a diverse range of pathogenic bacteria that can infect hosts across the plant kingdom. However, much of our current understanding of P. syringae is centered on its infection of flowering plants. We took a comparative approach to understand how P. syringae infects evolutionarily divergent plants. We identified P. syringae isolates causing disease in the liverwort Marchantia polymorpha, the fern Ceratopteris richardii, and the flowering plant Nicotiana benthamiana, which last shared a common ancestor >500 million years ago. Phytotoxin-enriched phylogroup (PG) 2 isolates of P. syringae are virulent in non-flowering plants, relying on type-3 effectors and the lipopeptide phytotoxin syringomycin. Ectopic syringomycin promotes tissue necrosis, activates conserved stress-related genes, and enhances in planta bacterial growth of toxin-deficient PGs in Marchantia. Collectively, our research reveals a key role for syringomycin in promoting Pseudomonas colonization, which works alongside effectors to antagonize an exceptionally wide spectrum of land plants.

Keywords: Ceratopteris richardii; Marchantia polymorpha; Nicotiana benthamiana; Pseudomonas syringae; evolution; lipopeptide toxin; necrosis; plant disease; plant pathogen; syringomycin.