Xanthomonas coordinates type III–type II effector synergy by activating fruit-ripening pathway.

Plant cell walls harbor vast carbohydrate reserves, yet how pathogens unlock them remains unclear. We show that the citrus canker pathogen Xanthomonas citri subsp. citri (Xcc) mobilizes cell wall sugars by hijacking a fruit-ripening program through the type III effector PthA4, which activates the ripening coordinator CsLOB1. CsLOB1 induces approximately 100 genes, many encoding enzymes involved in cell wall breakdown. In the nonfruiting species Nicotiana benthamiana, CsLOB1 likewise promotes Xanthomonas growth, showing that its activity is not strictly dependent on a ripening program. Transcriptomics and reporter assays revealed PthA4-dependent activation of the Xcc xylan CUT system, triggered by host-derived xylose and including a type II–secreted xylanase. Thus, PthA4-driven cell wall remodeling activates bacterial xylan use, establishing a TIII–TII effector feedforward loop that fuels Xcc proliferation. Editor's summary: Xanthomonas bacteria cause a range of necrotic diseases in plants, with substantial losses to agricultural yields. Two Research Articles in this issue report mechanisms by which Xanthomonas exploits plant molecular machinery to facilitate bacterial nutrition (see the Perspective by Kvitko and Jacobs). Wang et al. found that the Xanthomonas effector AvrBs2 uses plant-derived carbohydrates to synthesize a sugar phosphodiester called xanthosan. Other bacterial proteins export xanthosan to the extracellular space and hydrolyze xanthosan for bacterial metabolism. These results offer a xanthosan-based strategy for disease control. Phan et al. found that the effector PthA4 activates citrus fruit ripening to trigger the degradation of xylan. The authors provide insight into the interplay of bacterial proteins entering through different secretion systems. —Madeleine Seale [ABSTRACT FROM AUTHOR]