A bacterial derived plant- mimicking cytokinin hormone regulates social behaviour in a rice pathogen
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Evaluation Summary:
The major finding of this manuscript is that cytokinin produced by a bacterial plant pathogen affects bacterial growth and physiology. Production of cytokinin is linked to the well-known type three effector XopQ, which has primarily been studied for its function inside plant cells. The authors provide evidence that XopQ is required for the pathogen Xanthomonas oryzae to produce cytokinin in culture, and that cytokinin production controls whether or not the bacterium engages in planktonic growth or biofilm formation (i.e., biofilms form in the absence of cytokinin). These data indicate that bacterially produced cytokinins affect bacterial physiology, indicating that these hormones control signaling beyond photosynthetic organisms. The findings are of interest both to those studying plant-pathogen interactions and to microbiologists in general.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Many plant-associated bacteria produce plant- mimicking hormones which are involved in modulating host physiology. However, their function in modulating bacterial physiology has not been reported. Here we show that the XopQ protein, a type-III effector of the rice pathogen, Xanthomonas oryzae pv. oryzae ( Xoo ), is involved in cytokinin biosynthesis. Xoo produces and secretes an active form of cytokinin which enables the bacterium to maintain a planktonic lifestyle and promotes virulence. RNA-seq analysis indicates that the cytokinin produced by Xoo is required for the regulation of several genes which are involved in biofilm formation. We have also identified the Xoo isopentenyl transferase gene, which is involved in the cytokinin biosynthesis pathway and is required for maintaining planktonic behaviour and virulence. Furthermore, mutations in the predicted cytokinin receptor kinase (PcrK) and the downstream response regulator (PcrR) of Xoo phenocopy the cytokinin biosynthetic mutants, but are not complemented by supplementation with exogenous cytokinin. Cytokinin biosynthetic functions are encoded in a number of diverse bacterial genomes suggesting that cytokinin may be a widespread signalling molecule in the bacterial kingdom.
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Evaluation Summary:
The major finding of this manuscript is that cytokinin produced by a bacterial plant pathogen affects bacterial growth and physiology. Production of cytokinin is linked to the well-known type three effector XopQ, which has primarily been studied for its function inside plant cells. The authors provide evidence that XopQ is required for the pathogen Xanthomonas oryzae to produce cytokinin in culture, and that cytokinin production controls whether or not the bacterium engages in planktonic growth or biofilm formation (i.e., biofilms form in the absence of cytokinin). These data indicate that bacterially produced cytokinins affect bacterial physiology, indicating that these hormones control signaling beyond photosynthetic organisms. The findings are of interest both to those studying plant-pathogen interactions and to …
Evaluation Summary:
The major finding of this manuscript is that cytokinin produced by a bacterial plant pathogen affects bacterial growth and physiology. Production of cytokinin is linked to the well-known type three effector XopQ, which has primarily been studied for its function inside plant cells. The authors provide evidence that XopQ is required for the pathogen Xanthomonas oryzae to produce cytokinin in culture, and that cytokinin production controls whether or not the bacterium engages in planktonic growth or biofilm formation (i.e., biofilms form in the absence of cytokinin). These data indicate that bacterially produced cytokinins affect bacterial physiology, indicating that these hormones control signaling beyond photosynthetic organisms. The findings are of interest both to those studying plant-pathogen interactions and to microbiologists in general.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
In this manuscript, the authors present well-designed experimental data to demonstrate a bacterial T3SS effector, XopQ, encodes a phosphoribose-hydrolase to be involved in endogenous cytokinin (iP and tZ) biosynthesis. Inactivation of xopQ resulted in decrease of biofilm development and virulence, whereas addition of exogenous cytokinin rescued the phenotypic deficiencies of the mutant. They also found an ipt gene mutant of Xoo phenocopied xopQ mutation, reinforced the notion that Xoo synthesizes cytokinin with important role in the bacterial pathogen. In addition, the authors found that activation of bacterial cytokinin sensor pcrK and its cognate response regulator gene pcrR decreased virulence and biofilm, but addition of cytokinin cannot suppress the deficiencies of the pcrK or pcrR mutations. This work, …
Reviewer #1 (Public Review):
In this manuscript, the authors present well-designed experimental data to demonstrate a bacterial T3SS effector, XopQ, encodes a phosphoribose-hydrolase to be involved in endogenous cytokinin (iP and tZ) biosynthesis. Inactivation of xopQ resulted in decrease of biofilm development and virulence, whereas addition of exogenous cytokinin rescued the phenotypic deficiencies of the mutant. They also found an ipt gene mutant of Xoo phenocopied xopQ mutation, reinforced the notion that Xoo synthesizes cytokinin with important role in the bacterial pathogen. In addition, the authors found that activation of bacterial cytokinin sensor pcrK and its cognate response regulator gene pcrR decreased virulence and biofilm, but addition of cytokinin cannot suppress the deficiencies of the pcrK or pcrR mutations. This work, together with previous studies carried out in Xcc and M. tuberculosis, reveals that bacteria produce cytokinins, which were originally recognized as plant hormones, and modulate essential physiological processes of these pathogens. Cytokinin is an adenine derivate, and further studies will shed more light on this interesting topic.
Major comments:
1. The regulatory logic among XopQ, ipt and PcrR-PcrK is somewhat loose. Although XopQ and IPT seem in a pathway to synthesize cytokinin, the relationship between them and PcrRK is not established, especially with regard to endo- and exogenous cytokinin.
2. The author showed that bacterium Xoo synthesize more iP than tZ, but does tZ rescue deficiencies in producing biofilm and virulence?
3. The authors suggested that the IPT gene of Xoo is likely originated from HGT; are there more data on its possible origin?
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Reviewer #2 (Public Review):
Prior to this work, it was known that plants and bacteria produced cytokinins, which affect plant physiology. This work provides new evidence that cytokinins produced by a plant pathogen affects bacterial physiology controlling free-living and biofilm states, which is a novel finding.
The strengths of the work include the use of genetic and quantitative assays to demonstrate that proteins associated with cytokinin biosynthesis and cytokinin sensing are required to maintain planktonic growth. The work is however descriptive and does not provide a mechanistic understanding of the role of cytokinin in the regulation of biofilm formation and type III secretion. The weakness is that the study does not include experiments addressing when cytokinin is produced (exponential growth, motility, stationary phase and …
Reviewer #2 (Public Review):
Prior to this work, it was known that plants and bacteria produced cytokinins, which affect plant physiology. This work provides new evidence that cytokinins produced by a plant pathogen affects bacterial physiology controlling free-living and biofilm states, which is a novel finding.
The strengths of the work include the use of genetic and quantitative assays to demonstrate that proteins associated with cytokinin biosynthesis and cytokinin sensing are required to maintain planktonic growth. The work is however descriptive and does not provide a mechanistic understanding of the role of cytokinin in the regulation of biofilm formation and type III secretion. The weakness is that the study does not include experiments addressing when cytokinin is produced (exponential growth, motility, stationary phase and viability) and biologically relevant concentrations of cytokinin that lead to the different states (free-living, biofilms, infectious state). More evidence supporting the concentration-dependent activity of cytokinin on bacterial physiology will strengthen the main observation reported, and help evaluate data where exogenous treatment with cytokinin led to unexpected phenotypes (e.g. wild-type bacterial cells + cytokinin produced more biofilm than untreated wild type bacterial cells).
The importance of this work is that it reveals new roles for cytokinins outside of the plant kingdom and highlights an additional complexity by which these hormones contribute to pathogenic and nonpathogenic states.
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