Journal Article

Comparative transcriptomics reveals a highly polymorphic Xanthomonas HrpG virulence regulon

Gagnevin, Lionel, Monnens, Thomas Quiroz, Jacques, Marie-Agnès, Lauber, Emmanuelle, Jardinaud, Marie-Françoise, Cunnac, Sébastien, Szurek, Boris, Koebnik, Ralf, Charbit, Erika, Boulanger, Alice, Roux, Brice, Darrasse, Armelle, Arlat, Matthieu, Pruvost, Olivier, Noël, Laurent D., Carrère, Sébastien

2024

Overview

Background Bacteria of the genus Xanthomonas cause economically significant diseases in various crops. Their virulence is dependent on the translocation of type III effectors (T3Es) into plant cells by the type III secretion system (T3SS), a process regulated by the master response regulator HrpG. Although HrpG has been studied for over two decades, its regulon across diverse Xanthomonas species, particularly beyond type III secretion, remains understudied. Results In this study, we conducted transcriptome sequencing to explore the HrpG regulons of 17 Xanthomonas strains, encompassing six species and nine pathovars, each exhibiting distinct host and tissue specificities. We employed constitutive expression of plasmid-borne hrpG *, which encodes a constitutively active form of HrpG, to induce the regulon. Our findings reveal substantial inter- and intra-specific diversity in the HrpG* regulons across the strains. Besides 21 genes directly involved in the biosynthesis of the T3SS, the core HrpG* regulon is limited to only five additional genes encoding the transcriptional activator HrpX, the two T3E proteins XopR and XopL, a major facility superfamily (MFS) transporter, and the phosphatase PhoC. Interestingly, genes involved in chemotaxis and genes encoding enzymes with carbohydrate-active and proteolytic activities are variably regulated by HrpG*. Conclusions The diversity in the HrpG* regulon suggests that HrpG-dependent virulence in Xanthomonas might be achieved through several distinct strain-specific strategies, potentially reflecting adaptation to diverse ecological niches. These findings enhance our understanding of the complex role of HrpG in regulating various virulence and adaptive pathways, extending beyond T3Es and the T3SS.

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Analysis / Animal Genetics and Genomics / Annotations / Bacteria, Phytopathogenic / Bacterial Proteins - genetics / Bacterial Proteins - metabolism / Biomedical and Life Sciences / Biosynthesis / Carbohydrates / Chemotaxis / Coding / Control / Disease / DNA sequencing / Ecological niches / Gene Expression Profiling / Gene Expression Regulation, Bacterial / Genes / Genetic aspects / Genomes / Health aspects / HrpG / Identification and classification / Kinases / Life Sciences / Microarrays / Microbial Genetics and Genomics / Nucleotide sequencing / Pathogens / Phosphorylation / Phylogenetics / Physiology / Phytopathology and phytopharmacy / Plant cells / Plant Genetics and Genomics / Protein transport / Proteins / Proteolysis / Proteomics / Regulon / Regulon diversity / Reproducibility / Secretion / Sequences / Strains (organisms) / Transcription Factors - genetics / Transcription Factors - metabolism / Transcriptome / Transcriptome sequencing / Transcriptomes / Transcriptomics / Translocation / Type III secretion system / Type III Secretion Systems - genetics / Type III Secretion Systems - metabolism / Vegetal Biology / Virulence / Virulence (Microbiology) / Virulence - genetics / Xanthomonas / Xanthomonas - genetics / Xanthomonas - pathogenicity