Ralstonia pseudosolanacearumLOV domain protein regulates environmental stress tolerance, iron homeostasis, and bacterial wilt virulence
Abstract
Bacteria use diverse sensors to integrate environmental stimuli into physiological responses that ensure fitness and survival.Ralstonia pseudosolanacearum(Rps), a soil-borne plant pathogen that causes bacterial wilt disease, encodes a conserved LOV (light-oxygen-voltage) protein that mediates photoreception across the tree of life. However,Rpshad a minimal LOV-dependent transcriptional response to light in culture. Clues from functional domains, thelovgenomic neighborhood, and transcriptional analyses suggest that LOV shapesRpsbiology in response to stress. Loss of LOV did not affectRpsbiofilm or motilityin vitro, but did influence expression of genes encoding for these phenotypesin planta. TheΔlovmutant had reduced heat tolerance and broad metabolic dysregulation, leading to growth defects on several carbon sources but a growth advantage inex vivotomato xylem sap and in high-iron medium.In vitro, theΔlovmutant was more tolerant than wild type of redox stress and the antimicrobial phenolic caffeate, butRpsrequiredlovfor full virulence on tomato. LOV mediated attachment to the root surface, stem colonization, and overall symptom development. Together these findings reveal that LOV, which is highly conserved among plant pathogenicRalstonia, modulatesRpsstress response and virulence independently of light cues, but in a plant-dependent fashion.
Importance
Like other plant-associated microbes, the destructive crop pathogenRalstonia pseudosolanacearum(Rps) must integrate a complex array of biotic and abiotic signals to successfully infect and colonize the roots and xylem vessels of its plant hosts.Rpsencodes a large LOV domain protein. LOV proteins sense blue light in leaf colonizing microbes, butRpsinhabits soil, plant roots, and xylem where there is little blue light. Although deletinglovhad only minor effects when the bacterium grew in culture, many genes were dysregulated when theΔlovmutant infected tomato plants. Functional experiments showed LOV has diverse light-independent roles inRps, including modulating environmental stress tolerance and cellular iron and redox status. Most importantly,Rpsneeds LOV to grow normally in plants and cause bacterial wilt disease. Thus, LOV is a key sensor-regulator that controlsRpsadaptation to the plant environment and virulence.
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