The transcriptome analysis of the Arabidopsis thaliana in response to the Vibrio vulnificus by RNA-sequencing

Autoři: Yong-Soon Park aff001;  Seon-Kyu Kim aff003;  Seon-Young Kim aff004;  Kyung Mo Kim aff005;  Choong-Min Ryu aff002
Působiště autorů: Biotechnology Research Institute, College of Natural Sciences, Chungbuk National University, Cheongju, South Korea aff001;  Molecular Phytobacteriology Laboratory, Infection Disease Research Center, KRIBB, Daejeon, South Korea aff002;  Personalized Genomic Medicine Research Center, KRIBB, Daejeon, South Korea aff003;  Genome Editing Research Center, KRIBB, Daejeon, South Korea aff004;  Department of Functional Genomics, University of Science and Technology (UST), Daejeon, South Korea aff005;  Microbial Resource Center, KRIBB, Jeongeup, South Korea aff006;  Biosystem and Bioengineering Program, University of Science and Technology (UST), Daejeon, South Korea aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225976


Because of the recent increase in the demand for fresh produce, contamination of raw food products has become an issue. Foodborne diseases are frequently caused by the infection of leguminous plants by human bacterial pathogens. Moreover, contamination by Vibrio cholerae, closely related with Vibrio vulnificus, has been reported in plants and vegetables. Here, we investigated the possibility of Vibrio vulnificus 96-11-17M, an opportunistic human pathogen, to infect and colonize Arabidopsis thaliana plants, resulting in typical disease symptoms at 5 and 7 days post-inoculation in vitro and in planta under artificial and favorable conditions, respectively. RNA-Seq analysis revealed 5,360, 4,204, 4,916 and 3,741 differentially expressed genes (DEGs) at 12, 24, 48 and 72 h post-inoculation, respectively, compared with the 0 h time point. Gene Ontology analysis revealed that these DEGs act in pathways responsive to chemical and hormone stimuli and plant defense. The expression of genes involved in salicylic acid (SA)-, jasmonic acid (JA)- and ethylene (ET)-dependent pathways was altered following V. vulnificus inoculation. Genetic analyses of Arabidopsis mutant lines verified that common pathogen-associated molecular pattern (PAMP) receptors perceive the V. vulnificus infection, thus activating JA and ET signaling pathways. Our data indicate that the human bacterial pathogen V. vulnificus 96-11-17M modulates defense-related genes and host defense machinery in Arabidopsis thaliana under favorable conditions.

Klíčová slova:

Arabidopsis thaliana – Gene expression – Leaves – Plant bacterial pathogens – Plant pathology – Population density – Pseudomonas syringae – Vibrio vulnificus


1. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot. 2004; 67: 2342–2353. doi: 10.4315/0362-028x-67.10.2342 15508656

2. Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens, Environ Microbiol. 2010; 12: 2385–2397. doi: 10.1111/j.1462-2920.2010.02297.x 20636374

3. Fatica MK, Schneider KR. Salmonella and produce: survival in the plant environment and implications in food safety, Virulence. 2011; 2: 573–579. doi: 10.4161/viru.2.6.17880 21971184

4. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swrdlow DL. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982–2002, Emerg Infect Dis. 2005; 11: 603–609. doi: 10.3201/eid1104.040739 15829201

5. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States-major pathogens, Emerg Infect Dis. 2011; 17: 7–15. 21192848

6. Hussain MA, Dawson CO. Economic impact of food safety outbreaks on food businesses. Foods. 2013; 2: 585–589. doi: 10.3390/foods2040585 28239140

7. Lynch MF, Tauxe RV, Hedberg CM. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidermiol Infect. 2009; 137: 307–315.

8. Barak JD, Schroder BK. Interrelationships of food safety and plant pathology: the life cycle of human pathogens on plants. Annu Rev Phytopathol. 2012; 50: 241–266. doi: 10.1146/annurev-phyto-081211-172936 22656644

9. Seo KH, Frank JF. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J Food Prot. 1999; 62: 3–9. doi: 10.4315/0362-028x-62.1.3 9921820

10. Saldaña Z, Sánchez E, Xicohtencatl-Cortes J, Puente JL, Girón JA. Surface structures involved in plant stomata and leaf colonization by shiga-toxigenic Escherichia coli o157:h7. Front Microbiol. 2011; 2: 119. doi: 10.3389/fmicb.2011.00119 21887151

11. Blake PA, Merson MH, Weaver RE, Hollis DG, Heublein PC. Disease caused by a marine Vibrio. Clinical characteristics and epidemiology. N Engl J Med. 1979; 300: 1–5. doi: 10.1056/NEJM197901043000101 758155

12. Wright AC, Hill RT, Johnson JA, Roghman MC, Colwell RR, Morris JG. Distribution of Vibrio vulnificus in the Chesapeake Bay. Appl Environ Microbiol. 1996; 62: 717–724. 8593075

13. Heidelberg JF, Heidelberg KB, Colwell RR. Seasonality of Chesapeake Bay bacterioplankton species. Appl Environ Microbiol. 2002; 68: 5488–5497. doi: 10.1128/AEM.68.11.5488-5497.2002 12406742

14. Tison DL, Nishibuchi M, Greenwood JD, Seidler RJ. Vibrio vulnificus biogroup 2: new biogroup pathogenic for eels. Appl Environ Microbiol. 1982; 44: 640–646. 7138004

15. Bisharat N et al. Clinical, epidemiological, and microbiological features of Vibrio vulnificus biogroup 3 causing outbreaks of wound infection and bacteraemia in Israel. Lancet. 1999; 354: 1421–1424. doi: 10.1016/s0140-6736(99)02471-x 10543668

16. Martin SJ, Siebeling RJ. Identification of Vibrio vulnificus O serovars with antilipopolysaccharide monoclonal antibody. J Clin Microbiol. 1991; 29: 1684–1688. 1761690

17. Biosca EG, Oliver JD, Amaro C. Phenotypic characterization of Vibrio vulnificus biotype 2, a lipopolysaccharide-based homogenous O serogroup within Vibrio vulnificus. Appl Environ Microbiol. 1996; 62: 918–927. 8975619

18. Hlady WG, Klontz KC. The epidemiology of Vibrio infections in Florida, 1981–1993. J Infect Dis. 1996; 173: 1176–1183. doi: 10.1093/infdis/173.5.1176 8627070

19. Thompson CC, Vicente AC, Souza RC, Vasconcelos AT, Vesth T, Alves N Jr, et al. Genomic taxonomy of Vibrios. BMC Evol Biol. 2009; 9: 258. doi: 10.1186/1471-2148-9-258 19860885

20. Koch WH, Payne WL, Wentz BA, Cebula TA. Rapid polymerase chain reaction method for detection of Vibrio cholerae in foods. Appl Environ Microbiol. 1993; 59: 556–560. 8434922

21. Huat JT, Leong YK, Lian HH. Laboratory study of Vibrio cholerae O1 survival on three types of boiled rice (Oryza sativa L.) held at room temperature. J Food Prot. 2008; 71: 2453–2459. doi: 10.4315/0362-028x-71.12.2453 19244898

22. Mrityunjoy A, Kaniz F, Fahmida J, Shanzida JS, Aftab U Md., Rashed N. Prevalence of Vibrio cholerae in different food samples in the city of Dhaka, Bangladesh. Int Food Res J. 2013; 20: 1017–1022.

23. Hounmanou YM, Mdegela RH, Dougnon TV, Mhongole OJ, Mayila ES, Malakalinga J, et al. Toxigenic Vibrio cholerae O1 in vegetables and fish raised in wastewater irrigated fields and stabilization ponds during a non-cholera outbreak period in Morogoro, Tanzania: an environmental health study. BMC Res Notes. 2016; 9: 466. doi: 10.1186/s13104-016-2283-0 27756420

24. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM. Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS One. 2012; 7: e48744. doi: 10.1371/journal.pone.0048744 23209558

25. Eisen MM, Spellman PT, Brown PO, Bostein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998; 95: 14863–14868. doi: 10.1073/pnas.95.25.14863 9843981

26. Motes ML et al. Influence of water temperature and salinity on Vibrio vulnificus in Northen Gulf and Atlantic Coast Oysters (Crassostrea virginica). Appl Environ Microbiol. 1998; 64: 1459–1465. 9546182

27. Huehn S et al. Pathogenic vibrios in environmental, seafood and clinical sources in Germany.Int J Med Microbiol. 2014; 304: 843–850. doi: 10.1016/j.ijmm.2014.07.010 25129553

28. Jones MK, Oliver JD. Vibrio vulnificus: disease and pathogenesis. Infect Immun. 2009; 77: 1723–1733. doi: 10.1128/IAI.01046-08 19255188

29. Visnovitz T, Solti A, Csikós G, Fricke W. Plasma membrane H(+) -ATPase gene expression, protein level and activity in growing and non-growing regions of barley (Hordeum vulgare) leaves. Physiol Plant. 2012; 144: 382–393. doi: 10.1111/j.1399-3054.2012.01578.x 22257033

30. Jeong HG, Oh MH, Kim BS, Lee MY, Han HJ, Choi SH. The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun. 2009; 77: 3209–3217. doi: 10.1128/IAI.00109-09 19487477

31. Bigeard J, Colcombet J, Hirt H. Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant. 2015; 8: 521–539. doi: 10.1016/j.molp.2014.12.022 25744358

32. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol.2005; 43: 205–227. doi: 10.1146/annurev.phyto.43.040204.135923 16078883

Článek vyšel v časopise


2019 Číslo 12