Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor

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 bacterio...

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Autores principales: Bonomi, H.R., Toum, L., Sycz, G., Sieira, R., Toscani, A.M., Gudesblat, G.E., Leskow, F.C., Goldbaum, F.A., Vojnov, A.A., Malamud, F.
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_1469221X_v17_n11_p1565_Bonomi
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spelling todo:paper_1469221X_v17_n11_p1565_Bonomi2023-10-03T16:17:29Z Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor Bonomi, H.R. Toum, L. Sycz, G. Sieira, R. Toscani, A.M. Gudesblat, G.E. Leskow, F.C. Goldbaum, F.A. Vojnov, A.A. Malamud, F. bathy-type phytochrome infection plant defenses transcriptional regulation virulence factors bacteriophytochrome exopolysaccharide phytochrome unclassified drug virulence factor xanthan bacterial polysaccharide bacterial protein phytochrome amino terminal sequence Article bacterial virulence biofilm carbohydrate synthesis carboxy terminal sequence controlled study far red light illumination light nonhuman photoreceptor plant defense priority journal sequence analysis Xanthomonas campestris biosynthesis crop gene expression regulation genetics growth, development and aging high throughput sequencing light metabolism microbiology mutation pathogenicity plant disease Xanthomonas campestris Bacterial Proteins Biofilms Crops, Agricultural Gene Expression Regulation, Bacterial High-Throughput Nucleotide Sequencing Light Mutation Phytochrome Plant Diseases Polysaccharides, Bacterial Virulence Factors Xanthomonas campestris 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. © 2016 The Authors Fil:Gudesblat, G.E. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Vojnov, A.A. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Malamud, F. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_1469221X_v17_n11_p1565_Bonomi
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic bathy-type phytochrome
infection
plant defenses
transcriptional regulation
virulence factors
bacteriophytochrome
exopolysaccharide
phytochrome
unclassified drug
virulence factor
xanthan
bacterial polysaccharide
bacterial protein
phytochrome
amino terminal sequence
Article
bacterial virulence
biofilm
carbohydrate synthesis
carboxy terminal sequence
controlled study
far red light
illumination
light
nonhuman
photoreceptor
plant defense
priority journal
sequence analysis
Xanthomonas campestris
biosynthesis
crop
gene expression regulation
genetics
growth, development and aging
high throughput sequencing
light
metabolism
microbiology
mutation
pathogenicity
plant disease
Xanthomonas campestris
Bacterial Proteins
Biofilms
Crops, Agricultural
Gene Expression Regulation, Bacterial
High-Throughput Nucleotide Sequencing
Light
Mutation
Phytochrome
Plant Diseases
Polysaccharides, Bacterial
Virulence Factors
Xanthomonas campestris
spellingShingle bathy-type phytochrome
infection
plant defenses
transcriptional regulation
virulence factors
bacteriophytochrome
exopolysaccharide
phytochrome
unclassified drug
virulence factor
xanthan
bacterial polysaccharide
bacterial protein
phytochrome
amino terminal sequence
Article
bacterial virulence
biofilm
carbohydrate synthesis
carboxy terminal sequence
controlled study
far red light
illumination
light
nonhuman
photoreceptor
plant defense
priority journal
sequence analysis
Xanthomonas campestris
biosynthesis
crop
gene expression regulation
genetics
growth, development and aging
high throughput sequencing
light
metabolism
microbiology
mutation
pathogenicity
plant disease
Xanthomonas campestris
Bacterial Proteins
Biofilms
Crops, Agricultural
Gene Expression Regulation, Bacterial
High-Throughput Nucleotide Sequencing
Light
Mutation
Phytochrome
Plant Diseases
Polysaccharides, Bacterial
Virulence Factors
Xanthomonas campestris
Bonomi, H.R.
Toum, L.
Sycz, G.
Sieira, R.
Toscani, A.M.
Gudesblat, G.E.
Leskow, F.C.
Goldbaum, F.A.
Vojnov, A.A.
Malamud, F.
Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
topic_facet bathy-type phytochrome
infection
plant defenses
transcriptional regulation
virulence factors
bacteriophytochrome
exopolysaccharide
phytochrome
unclassified drug
virulence factor
xanthan
bacterial polysaccharide
bacterial protein
phytochrome
amino terminal sequence
Article
bacterial virulence
biofilm
carbohydrate synthesis
carboxy terminal sequence
controlled study
far red light
illumination
light
nonhuman
photoreceptor
plant defense
priority journal
sequence analysis
Xanthomonas campestris
biosynthesis
crop
gene expression regulation
genetics
growth, development and aging
high throughput sequencing
light
metabolism
microbiology
mutation
pathogenicity
plant disease
Xanthomonas campestris
Bacterial Proteins
Biofilms
Crops, Agricultural
Gene Expression Regulation, Bacterial
High-Throughput Nucleotide Sequencing
Light
Mutation
Phytochrome
Plant Diseases
Polysaccharides, Bacterial
Virulence Factors
Xanthomonas campestris
description 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. © 2016 The Authors
format JOUR
author Bonomi, H.R.
Toum, L.
Sycz, G.
Sieira, R.
Toscani, A.M.
Gudesblat, G.E.
Leskow, F.C.
Goldbaum, F.A.
Vojnov, A.A.
Malamud, F.
author_facet Bonomi, H.R.
Toum, L.
Sycz, G.
Sieira, R.
Toscani, A.M.
Gudesblat, G.E.
Leskow, F.C.
Goldbaum, F.A.
Vojnov, A.A.
Malamud, F.
author_sort Bonomi, H.R.
title Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
title_short Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
title_full Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
title_fullStr Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
title_full_unstemmed Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
title_sort xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor
url http://hdl.handle.net/20.500.12110/paper_1469221X_v17_n11_p1565_Bonomi
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