Transcriptome analysis of Xanthomonas oryzae pv. oryzicola exposed to H2O2 reveals horizontal gene transfer contributes to its oxidative stress response

Autoři: Yuan Fang aff001;  Haoye Wang aff001;  Xia Liu aff001;  Dedong Xin aff001;  Yuchun Rao aff001;  Bo Zhu aff002
Působiště autorů: College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, P.R. China aff001;  School of Agriculture and Biology, Shanghai Jiao Tong University/Key Laboratory of Urban Agriculture by Ministry of Agriculture of China, Shanghai, China aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Xanthomonas oryzae pv. oryzicola (Xoc), the causal agent of bacterial leaf streak, is one of the most severe seed-borne bacterial diseases of rice. However, the molecular mechanisms underlying Xoc in response to oxidative stress are still unknown. In this study, we performed a time-course RNA-seq analysis on the Xoc in response to H2O2, aiming to reveal its oxidative response network. Overall, our RNA sequence analysis of Xoc revealed a significant global gene expression profile when it was exposed to H2O2. There were 7, 177, and 246 genes that were differentially regulated at the early, middle, and late stages after exposure, respectively. Three genes (xoc_1643, xoc_1946, xoc_3249) showing significantly different expression levels had proven relationships with oxidative stress response and pathogenesis. Moreover, a hypothetical protein (XOC_2868) showed significantly differential expression, and the xoc_2868 mutants clearly displayed a greater H2O2 sensitivity and decreased pathogenicity than those of the wild-type. Gene localization and phylogeny analysis strongly suggests that this gene may have been horizontally transferred from a Burkholderiaceae ancestor. Our study not only provides a first glance of Xoc’s global response against oxidative stress, but also reveals the impact of horizontal gene transfer in the evolutionary history of Xoc.

Klíčová slova:

Gene expression – Gene regulation – Oxidative stress – Pathogenesis – Plant bacterial pathogens – Plant pathogens – Rice – Xanthomonas


1. Liang X, Duan Y, Yu X, Wang J, Zhou M. Photochemical degradation of bismerthiazol: structural characterisation of the photoproducts and their inhibitory activities against Xanthomonas oryzae pv. oryzae. Pest Manag Sci. 2016; 72; 997–1003. doi: 10.1002/ps.4080 26174501

2. Ryan RP, Vorhölter FJ, Potnis N, Jones JB, Van Sluys MA, Bogdanove AJ, et al. Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat Rev Microbiol. 2011; 9; 344–355. doi: 10.1038/nrmicro2558 21478901

3. Niño-Liu DO, Ronald PC, Bogdanove AJ. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol. 2006; 7; 303–324. doi: 10.1111/j.1364-3703.2006.00344.x 20507449

4. Wojtaszek P. Oxidative burst: an early plant response to pathogen infection. Biochem J. 1997; 322; 681–692. doi: 10.1042/bj3220681 9148737

5. Doke N, Miura Y, Sanchez LM, Park HJ, Noritake T, Yoshioka H, et al. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence—a review. Gene 1996; 179; 45–51. doi: 10.1016/s0378-1119(96)00423-4 8955628

6. Torres MA, Jones JDG, Dangl JL. Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet. 2005; 37; 1130–1134. doi: 10.1038/ng1639 16170317

7. Liochev SI. Reactive oxygen species and the free radical theory of aging. Free Radic Biol Med. 2013; 60; 1–4. doi: 10.1016/j.freeradbiomed.2013.02.011 23434764

8. Manlu Z, Xiongfeng D. Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress. Nucleic Acids Res. 2019; doi: 10.1093/nar/gkz467 31131413

9. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol. 2013;11;443–454. doi: 10.1038/nrmicro3032 23712352

10. Imlay JA. Transcription factors that defend bacteria against reactive oxygen species. Annu Rev Microbiol. 2015; 69;93–108. doi: 10.1146/annurev-micro-091014-104322 26070785

11. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, Yu L, et al. A strand-specific RNA–Seq analysis of the transcriptome of the typhoid Bacillus salmonella typhi. PLoS Genet. 2009; 5; e1000569. doi: 10.1371/journal.pgen.1000569 19609351

12. Shimizu R, Chou K, Orita I, Suzuki Y, Nakamura S, Fukui T. Detection of phase-dependent transcriptomic changes and Rubisco-mediated CO2 fixation into poly (3-hydroxybutyrate) under heterotrophic condition in Ralstonia eutropha H16 based on RNA-seq and gene deletion analyses. BMC Microbiol. 2013; 13; 169. doi: 10.1186/1471-2180-13-169 23879744

13. Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV, Patil PB et al. Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol. 2011; 193; 5450–5464. doi: 10.1128/JB.05262-11 21784931

14. Upadhya R, Campbell LT, Donlin MJ, Aurora R, Lodge JK. Global transcriptome profile of Cryptococcus neoformans during exposure to hydrogen peroxide induced oxidative stress. PLoS ONE 2013; 8; e55110. doi: 10.1371/journal.pone.0055110 23383070

15. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10; R25. doi: 10.1186/gb-2009-10-3-r25 19261174

16. Maza E. In papyro comparison of TMM (edgeR), RLE (DESeq2), and MRN normalization methods for a simple Two-Conditions-Without-Replicates RNA-Seq experimental design. Front Genet. 2016; 16; 164.

17. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26; 139–140. doi: 10.1093/bioinformatics/btp616 19910308

18. de Hoon MJL, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004; 20; 1453–1454. doi: 10.1093/bioinformatics/bth078 14871861

19. Jozefczuk J, James A. Chapter Six—Quantitative real-time PCR-based analysis of gene expression. Methods Enzymol. 2011;500;99–109. doi: 10.1016/B978-0-12-385118-5.00006-2

20. Guo W, Cai LL, Zou H-S, Ma WX, Liu XL, Zou LF, et al. Ketoglutarate transport protein KgtP is secreted through the type III secretion system and contributes to virulence in Xanthomonas oryzae pv. oryzae. Appl Environ Microbiol. 2012; 78; 5672–5681. doi: 10.1128/AEM.07997-11 22685129

21. Qian G, Liu C, Wu G, Yin F, Zhao Y, Zhou Y, et al. AsnB, regulated by diffusible signal factor and global regulator Clp, is involved in aspartate metabolism, resistance to oxidative stress and virulence in Xanthomonas oryzae pv. oryzicola. Mol Plant Pathol. 2013; 14; 145–157. doi: 10.1111/j.1364-3703.2012.00838.x 23157387

22. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30; 772–780. doi: 10.1093/molbev/mst010 23329690

23. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010; 59; 307–321. doi: 10.1093/sysbio/syq010 20525638

24. Berghoff BA, Konzer A, Mank NN, Looso M, Rische T, Forstner KU, et al. Integrative “omics”-approach discovers dynamic and regulatory features of bacterial stress responses. PLoS Genet. 2013; 9; e1003576. doi: 10.1371/journal.pgen.1003576 23818867

25. Nobre LS, Saraiva LM. Effect of combined oxidative and nitrosative stresses on Staphylococcus aureus transcriptome. Appl Microbiol Biotechnol. 2013; 97; 2563–2573. doi: 10.1007/s00253-013-4730-3 23389340

26. Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, Botella E, et al. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 2012; 335; 1099–1103. doi: 10.1126/science.1206871 22383848

27. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 2014; 43; 447–452.

28. Rice WR. Analyzing tables of statistical tests. Evolution 1989; 43; 223–225. doi: 10.1111/j.1558-5646.1989.tb04220.x 28568501

29. Ballouz S, Francis AR, Lan R, Tanaka MM. Conditions for the evolution of gene clusters in bacterial genomes. PLoS Comput Biol. 2010; 6; e1000672. doi: 10.1371/journal.pcbi.1000672 20168992

30. Mongkolsuk S, Whangsuk W, Vattanaviboon P, Loprasert S, Fuangthong M. A Xanthomonas alkyl hydroperoxide reductase subunit C (ahpC) mutant showed an altered peroxide stress response and complex regulation of the compensatory response of peroxide detoxification enzymes. J Bacteriol. 2000; 182; 6845–6849. doi: 10.1128/jb.182.23.6845-6849.2000 11073935

31. Nachin L, Loiseau L, Expert D, Barras F. SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe—S] biogenesis under oxidative stress. The EMBO J. 2003; 22; 427–437. doi: 10.1093/emboj/cdg061 12554644

32. Blanvillain S, Meyer D, Boulanger A, Lautier M, Guynet C, Denancé N, et al. Plant carbohydrate scavenging through TonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS ONE 2007; 2; e224. doi: 10.1371/journal.pone.0000224 17311090

33. Horsburgh MJ, Wharton SJ, Cox AG, Ingham E, Peacock S, Foster SJ. MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol. 2002; 44; 1269–1286. doi: 10.1046/j.1365-2958.2002.02944.x 12028379

34. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000; 405; 299–304. doi: 10.1038/35012500 10830951

35. Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 2008; 9; 605–618. doi: 10.1038/nrg2386 18591983

36. Kim HS, Park HJ, Heu S, Jung J. Molecular and functional characterization of a unique sucrose hydrolase from Xanthomonas axonopodis pv. glycines. J Bacteriol. 2004; 186; 411–418. doi: 10.1128/JB.186.2.411-418.2004 14702310

37. Duwat P, Ehrlich SD, Gruss A. Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol Microbiol. 1999; 31: 845–858. doi: 10.1046/j.1365-2958.1999.01222.x 10048028

38. Hu P, Brodie EL, Suzuki Y, McAdams HH, Andersen GL. Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Bacteriol. 2005; 187; 8437–8449. doi: 10.1128/JB.187.24.8437-8449.2005 16321948

39. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 2002; 82; 187–216. 12369188

40. Jo K, Kwon H-B, Kim S. Time-series RNA-seq analysis package (TRAP) and its application to the analysis of rice, Oryza sativa L. ssp. Japonica, upon drought stress. Methods 2014; 67; 364–372. doi: 10.1016/j.ymeth.2014.02.001 24518221

41. Wu J, Weiss B. Two divergently transcribed genes, soxR and soxS, control a superoxide response regulon of Escherichia coli. J Bacteriol. 1991; 173; 2864–2871. doi: 10.1128/jb.173.9.2864-2871.1991 1708380

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden