Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae

ABSTRACT Xanthomonas is a notorious plant pathogen causing serious diseases in hundreds of plant hosts. Xanthomonas species are equipped with an array of signal transduction systems that regulate gene expression to survive in various harsh environments and successfully infect hosts. Although certain...

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Autores principales: Dehong Zheng, Huihui Wang, Hao Zhong, Wenli Ke, Huifeng Hu, Ming Sun, Lifang Ruan
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:5d5c1c6aaf27496081e5c3976b1694842021-12-02T19:22:27ZElucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae10.1128/mSystems.00789-202379-5077https://doaj.org/article/5d5c1c6aaf27496081e5c3976b1694842021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00789-20https://doaj.org/toc/2379-5077ABSTRACT Xanthomonas is a notorious plant pathogen causing serious diseases in hundreds of plant hosts. Xanthomonas species are equipped with an array of signal transduction systems that regulate gene expression to survive in various harsh environments and successfully infect hosts. Although certain pathogenicity-associated regulators have been functionally characterized, signal transduction systems always function as a regulatory network which remains to be elucidated in Xanthomonas. This study used a systematic approach to characterize all identified pathogenicity-associated regulators in Xanthomonas oryzae pv. oryzae (Xoo), including a transcriptional regulator with unknown function, and their interactive regulatory network. RNA sequencing was used in elucidating the patterns of the 10 pathogenicity-associated regulators identified. Results revealed that each pathogenicity-associated regulator has cross talk with others and all these regulators function as a regulatory network, with VemR and PXO_RS20790 being the master pathogenicity-associated regulators and HrpX being the final executant. Moreover, regulome analysis showed that numerous genes other than genes in pathogenicity islands are finely regulated within the regulatory network. Given that most of the pathogenicity-associated regulators are conserved in Xanthomonadales, our findings suggest a global network of gene regulation in this evolutionarily conserved pathogen. In conclusion, our study provides essential basic information about the regulatory network in Xoo, suggesting that this complicated regulatory network is one of the reasons for the robustness and fitness of Xanthomonas spp. IMPORTANCE The host plant infection process of pathogenic bacteria is a coordinating cellular behavior, which requires dynamic regulation at several levels in response to variations in host plants or fluctuations in the external environment. As one of the most important genera of plant-pathogenic bacteria, Xanthomonas has been studied as a model. Although certain pathogenicity-associated regulators have been functionally characterized, interactions among them remain to be elucidated. This study systematically characterized pathogenicity-associated regulators in Xoo and revealed that cross talk exists among pathogenicity-associated regulators and function as a regulatory network in which a hierarchy exists among the regulators. Our study elucidated the landscape of the pathogenicity-associated regulatory network in Xanthomonas, promoting understanding of the infection process of pathogenic bacteria.Dehong ZhengHuihui WangHao ZhongWenli KeHuifeng HuMing SunLifang RuanAmerican Society for Microbiologyarticletwo-component signal transduction systemXanthomonasglobal regulatory networkspathogenicity regulationtranscription factorsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution DOAJ
collection DOAJ
language EN
topic two-component signal transduction system
Xanthomonas
global regulatory networks
pathogenicity regulation
transcription factors
Microbiology
QR1-502
spellingShingle two-component signal transduction system
Xanthomonas
global regulatory networks
pathogenicity regulation
transcription factors
Microbiology
QR1-502
Dehong Zheng
Huihui Wang
Hao Zhong
Wenli Ke
Huifeng Hu
Ming Sun
Lifang Ruan
Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
description ABSTRACT Xanthomonas is a notorious plant pathogen causing serious diseases in hundreds of plant hosts. Xanthomonas species are equipped with an array of signal transduction systems that regulate gene expression to survive in various harsh environments and successfully infect hosts. Although certain pathogenicity-associated regulators have been functionally characterized, signal transduction systems always function as a regulatory network which remains to be elucidated in Xanthomonas. This study used a systematic approach to characterize all identified pathogenicity-associated regulators in Xanthomonas oryzae pv. oryzae (Xoo), including a transcriptional regulator with unknown function, and their interactive regulatory network. RNA sequencing was used in elucidating the patterns of the 10 pathogenicity-associated regulators identified. Results revealed that each pathogenicity-associated regulator has cross talk with others and all these regulators function as a regulatory network, with VemR and PXO_RS20790 being the master pathogenicity-associated regulators and HrpX being the final executant. Moreover, regulome analysis showed that numerous genes other than genes in pathogenicity islands are finely regulated within the regulatory network. Given that most of the pathogenicity-associated regulators are conserved in Xanthomonadales, our findings suggest a global network of gene regulation in this evolutionarily conserved pathogen. In conclusion, our study provides essential basic information about the regulatory network in Xoo, suggesting that this complicated regulatory network is one of the reasons for the robustness and fitness of Xanthomonas spp. IMPORTANCE The host plant infection process of pathogenic bacteria is a coordinating cellular behavior, which requires dynamic regulation at several levels in response to variations in host plants or fluctuations in the external environment. As one of the most important genera of plant-pathogenic bacteria, Xanthomonas has been studied as a model. Although certain pathogenicity-associated regulators have been functionally characterized, interactions among them remain to be elucidated. This study systematically characterized pathogenicity-associated regulators in Xoo and revealed that cross talk exists among pathogenicity-associated regulators and function as a regulatory network in which a hierarchy exists among the regulators. Our study elucidated the landscape of the pathogenicity-associated regulatory network in Xanthomonas, promoting understanding of the infection process of pathogenic bacteria.
format article
author Dehong Zheng
Huihui Wang
Hao Zhong
Wenli Ke
Huifeng Hu
Ming Sun
Lifang Ruan
author_facet Dehong Zheng
Huihui Wang
Hao Zhong
Wenli Ke
Huifeng Hu
Ming Sun
Lifang Ruan
author_sort Dehong Zheng
title Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
title_short Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
title_full Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
title_fullStr Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
title_full_unstemmed Elucidation of the Pathogenicity-Associated Regulatory Network in <named-content content-type="genus-species">Xanthomonas oryzae</named-content> pv. oryzae
title_sort elucidation of the pathogenicity-associated regulatory network in <named-content content-type="genus-species">xanthomonas oryzae</named-content> pv. oryzae
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/5d5c1c6aaf27496081e5c3976b169484
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