AraC-Family Transcriptional Regulator WhpR Controls Virulence in Pseudomonas savastanoi pv. savastanoi Through Regulation of Indole Metabolism.

The Pseudomonas syringae complex WHOP genomic island underpins virulence in woody hosts by mediating the catabolism of aromatic compounds. However, the biochemical functions of the ipoABC and dhoAB operons and the regulatory gene whpR remain unknown. Comparative genomics revealed WHOP-like clusters beyond P. syringae, found in diverse plant-associated, environmental and clinical bacteria, including indole degraders. We propose that ipoABC and dhoAB mediate indole degradation via anthranilate, linking indole detoxification to central metabolism through the β-ketoadipate pathway. In the olive pathogen P. savastanoi pv. savastanoi, ipoABC promotes indole degradation, indigo production, cell aggregation and biofilm formation. WhpR, an AraC-family regulator structurally related to CuxR and ToxT, defines a regulon comprising repression of most WHOP operons along with genes outside this region, including trpAB, reflecting integrated regulation of indole catabolism and tryptophan biosynthesis. In line with the observed transcriptional repression of WHOP genes, deletion of whpR led to hypervirulence and significantly altered bacterial fitness in woody olive plants. These findings define the WHOP region as a regulatory hub linking indole detoxification, multicellular behaviour and virulence, emerging as a target for novel control strategies against woody plant diseases.