Abstract
Recent studies have demonstrated that an appropriate light environment is required for the establishment of efficient vegetal resistance responses in several plant-pathogen interactions. The photoreceptors implicated in such responses are mainly those belonging to the phytochrome family. Data obtained from bacterial genome sequences revealed the presence of photosensory proteins of the BLUF (Blue Light sensing Using FAD), LOV (Light, Oxygen, Voltage) and phytochrome families with no known functions. Xanthomonas axonopodis pv. citri is a Gram-negative bacterium responsible for citrus canker. The in silico analysis of the X. axonopodis pv. citri genome sequence revealed the presence of a gene encoding a putative LOV photoreceptor, in addition to two genes encoding BLUF proteins. This suggests that blue light sensing could play a role in X. axonopodis pv. citri physiology. We obtained the recombinant Xac-LOV protein by expression in Escherichia coli and performed a spectroscopic analysis of the purified protein, which demonstrated that it has a canonical LOV photochemistry. We also constructed a mutant strain of X. axonopodis pv. citri lacking the LOV protein and found that the loss of this protein altered bacterial motility, exopolysaccharide production and biofilm formation. Moreover, we observed that the adhesion of the mutant strain to abiotic and biotic surfaces was significantly diminished compared to the wild-type. Finally, inoculation of orange (Citrus sinensis) leaves with the mutant strain of X. axonopodis pv. citri resulted in marked differences in the development of symptoms in plant tissues relative to the wild-type, suggesting a role for the Xac-LOV protein in the pathogenic process. Altogether, these results suggest the novel involvement of a photosensory system in the regulation of physiological attributes of a phytopathogenic bacterium. A functional blue light receptor in Xanthomonas spp. has been described for the first time, showing an important role in virulence during citrus canker disease.
Highlights
Light is a major environmental stimulus that regulates plant physiology
In X. axonopodis pv. citri, the LOV protein is encoded by the fixL gene, which we renamed as lov gene for clarification purposes
We identified the putative 235 and 210 promoter sequences of this gene and found a XVM2 element located 329 bp upstream of the start codon. This element has been shown to be involved in the induction of several genes related to the pathogenesis of X. axonopodis pv. citri [35]
Summary
Light is a major environmental stimulus that regulates plant physiology. The perception of light has been linked to numerous physiological responses in microorganisms such as pigment synthesis, DNA repair and biofilm formation [4]. Recent reports revealed that in many bacteria light governs important lifestyle decisions, especially that between a single-cell motile state and a multicellular surface-attached state [5]. The participation of light in the regulation of bacterial virulence was recently found in non-photosynthetic bacteria. The presence of light receptors across several bacterial taxa, including many species with no known photobiology, suggests that the visible light environment has an unexplored regulatory role in the biology of bacterial cells [4,6,7,8]
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