Elucidation of the Pathogenicity-Associated Regulatory Network in Xanthomonas oryzae pv. oryzae

Dehong Zheng; Huihui Wang; Hao Zhong; Wenli Ke; Huifeng Hu; Ming Sun; Lifang Ruan

doi:10.1128/mSystems.00789-20

Elucidation of the Pathogenicity-Associated Regulatory Network in Xanthomonas oryzae pv. oryzae

mSystems. 2021 Mar 9;6(2):e00789-20. doi: 10.1128/mSystems.00789-20.

Authors

Dehong Zheng^{1

2}, Huihui Wang¹, Hao Zhong¹, Wenli Ke¹, Huifeng Hu¹, Ming Sun¹, Lifang Ruan³

Affiliations

¹ State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China.
² State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Agriculture, Guangxi University, Nanning, People's Republic of China.
³ State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China ruanlifang@mail.hzau.edu.cn.

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.

Keywords: Xanthomonas; global regulatory networks; pathogenicity regulation; transcription factors; two-component signal transduction system.