Phevamine A, a small molecule that suppresses plant immune responses.

Abstract

Bacterial plant pathogens cause significant crop damage worldwide. They invade plant cells by producing a variety of virulence factors, including small-molecule toxins and phytohormone mimics. Virulence of the model pathogen <i>Pseudomonas syringae</i> pv. <i>tomato</i> DC3000 (<i>Pto</i>) is regulated in part by the sigma factor HrpL. Our study of the HrpL regulon identified an uncharacterized, three-gene operon in <i>Pto</i> that is controlled by HrpL and related to the <i>Erwinia hrp</i>-associated systemic virulence (<i>hsv</i>) operon. Here, we demonstrate that the <i>hsv</i> operon contributes to the virulence of <i>Pto</i> on <i>Arabidopsis thaliana</i> and suppresses bacteria-induced immune responses. We show that the <i>hsv</i>-encoded enzymes in <i>Pto</i> synthesize a small molecule, phevamine A. This molecule consists of l-phenylalanine, l-valine, and a modified spermidine, and is different from known small molecules produced by phytopathogens. We show that phevamine A suppresses a potentiation effect of spermidine and l-arginine on the reactive oxygen species burst generated upon recognition of bacterial flagellin. The <i>hsv</i> operon is found in the genomes of divergent bacterial genera, including ∼37% of <i>P. syringae</i> genomes, suggesting that phevamine A is a widely distributed virulence factor in phytopathogens. Our work identifies a small-molecule virulence factor and reveals a mechanism by which bacterial pathogens overcome plant defense. This work highlights the power of omics approaches in identifying important small molecules in bacteria-host interactions.