A Novel Plant Secondary Metabolite-Binding Gene Family Required for Full Virulence in Pectobacterium parvum.

Abstract

Pectobacterium parvum is an emerging phytopathogen causing aerial stem rot of potato. P. parvum has a broad host range, with Chinese cabbage as one of its important hosts. Through multi-omics analysis, we discovered a previously uncharacterized gene family highly expressed during in planta infection, designated the plant secondary metabolite-binding (PSMB) family. This family likely originated via horizontal gene transfer and underwent lineage-specific expansion in P. parvum, forming a four-paralog pathogenicity island. Structural modelling revealed that PSMB proteins resemble the rhizobial RhiA protein, though their function in phytopathogens has not been established. Biochemical assays demonstrated that the representative member, PSMB1a, binds defensive plant secondary metabolites (PSMs) with high affinity. PSMB1a binds the solanidine with submicromolar affinity (K_d = 0.103 μM) and exhibited approximately 100-fold higher affinity over salicylic acid (K_d = 9.23 ± 2.35 μM), indicating selectivity for specific PSMs. Functional studies demonstrated that PSMB1a enhances tolerance to defensive PSMs and contributes to virulence. Heterologous expression of PSMB1a in sister species P. polare enhanced PSM tolerance and virulence on Chinese cabbage, but suppressed bacterial proliferation under non-stress conditions. Conversely, deletion of the entire PSMB pathogenicity island in P. parvum attenuated virulence on potato stems, Chinese cabbage, and radish while increasing in vitro growth, confirming a trade-off between virulence contribution and basal fitness. These findings identify the PSMB family as a new class of virulence factors in Pectobacterium and reveal a specialized adaptive strategy in P. parvum that involves the binding of defensive PSMs to facilitate infection.