Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor

Abstract

Phytochromes constitute a major photoreceptor family found in plants, algae, fungi, and prokaryotes, including pathogens. Here, we report that Xanthomonas campestris pv. campestris (Xcc), the causal agent of black rot disease which affects cruciferous crops worldwide, codes for a functional bacteriophytochrome (XccBphP). XccBphP possesses an N-terminal PAS2-GAF-PHY photosensory domain triad and a C-terminal PAS9 domain as its output module. Our results show that illumination of Xcc, prior to plant infection, attenuates its virulence in an XccBphP-dependent manner. Moreover, in response to light, XccBphP downregulates xanthan exopolysaccharide production and biofilm formation, two known Xcc virulence factors. Furthermore, the XccbphP null mutant shows enhanced virulence, similar to that of dark-adapted Xcc cultures. Stomatal aperture regulation and callose deposition, both well-established plant defense mechanisms against bacterial pathogens, are overridden by the XccbphP strain. Additionally, an RNA-Seq analysis reveals that far-red light or XccBphP overexpression produces genomewide transcriptional changes, including the inhibition of several Xcc virulence systems. Our findings indicate that Xcc senses light through XccBphP, eliciting bacterial virulence attenuation via downregulation of bacterial virulence factors. The capacity of XccBphP to respond to light both in vitro and in vivo was abolished by a mutation on the conserved Cys13 residue. These results provide evidence for a novel bacteriophytochrome function affecting an infectious process.

Pseudomonas syringaepv. tomato exploits light signals to optimize virulence and colonization of leaves

“…citri (Kraiselburd et al, 2012) and Xanthomonas campestris pv. campestris (Bonomi et al, 2016). Light quality and intensity change over the daynight cycle.…”

Phytochrome mediated responses inAgrobacterium fabrum: growth, swimming, plant infection and interbacterial competition

“…Phytochromes sense light in the blue, red and far-red range of the visible spectrum. A large number of developmental effects are controlled by phytochromes in land plants (4) and fungi (5), and several examples of phytochrome effects in bacteria have been reported, including control of photosynthesis and infection of plants by plant pathogens (6-12). In a search for phytochrome responses of A. fabrum , however, knockout mutants were generated which had no apparent phenotype (13).…”

Time‐Resolved Energetics of Photoprocesses in Prokaryotic Phytochrome‐Related Photoreceptors

“…In this work, we investigated by PA and optical spectroscopy diverse phy and phy‐related proteins (Figure ): (1) the GAF3 (g3) domain of Synechocystis CBCR Slr 1393 , a red/green (R/G) photochromic and bi‐stable unit ( Slr 1393g3‐R and Slr 1393g3‐G); (2) Synechocystis Cph1, Sy Cph1, exhibiting the familiar red/far red (R/FR) photoconversion pattern ; (3) full‐length and truncated constructs of Xanthomonas campestris bacteriophytochrome ( Xcc BphP, here abbreviated as Xcp1 ), a Bathy‐phy with absorbance maxima at 684 nm ( Xcp1 ‐R) and 758 nm ( Xcp1 ‐FR) ; the truncated form comprises the PGP module ( Xcp1 PGP); (4) the truncated, 65 kDa form of Avena sativa phyA ( As phyA65) reconstituted with PΦB or PCB .…”