Multilocus sequence analysis of xanthomonads causing bacterial spot of tomato and pepper plants reveals strains generated by recombination among species and recent global spread of Xanthomonas gardneri

Applied and Environmental Microbiology

Volumn 81, Issue 4, 2015, Pages 1520-1529

  Timilsina, Sujan ^a,b   Jibrin, Mustafa O ^c   Potnis, Neha ^a   Minsavage, Gerald V ^a   Kebede, Misrak ^d   Schwartz, Allison ^e   Bart, Rebecca ^f   Staskawicz, Brian ^e   Boyer, Claudine ^g   Vallad, Gary E ^a,b   Pruvost, Olivier ^g   Jones, Jeffrey B ^a   Gossa, Erica M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c AHMADU BELLO UNIVERSITY   (Nigeria)

^d HARAMAYA UNIVERSITY   (Ethiopia)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Danforth Center   (United States)

^g UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; FRUITS; GEOGRAPHICAL DISTRIBUTION; POPULATION DISTRIBUTION;

GLOBAL DISTRIBUTION; HOUSEKEEPING GENE; MULTILOCUS SEQUENCE ANALYSIS; PATHOGEN POPULATIONS; PHYLOGENETIC RELATIONSHIPS; RECOMBINATION EVENTS; SPECIES COMPOSITION; XANTHOMONAS SPECIES;

BACTERIA;

BACTERIAL DISEASE; COMMUNITY COMPOSITION; DISEASE SPREAD; FRUIT; GENETIC VARIATION; MOLECULAR ANALYSIS; RECOMBINATION;

AFRICA; NEW ZEALAND; NORTH AMERICA; SOUTHEAST ASIA;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; XANTHOMONAS; XANTHOMONAS GARDNERI; XANTHOMONAS VESICATORIA;

BACTERIAL PROTEIN;

AFRICA; ASIA; CLASSIFICATION; GENETIC RECOMBINATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; NEW ZEALAND; PEPPER; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; TOMATO; WESTERN HEMISPHERE; XANTHOMONAS;

AFRICA; AMERICAS; ASIA; BACTERIAL PROTEINS; CAPSICUM; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; NEW ZEALAND; PHYLOGENY; PLANT DISEASES; RECOMBINATION, GENETIC; XANTHOMONAS;

EID: 84922051741     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03000-14     Document Type: Article

References (53)

1. Jones JB, Lacy GH, Bouzar H, Stall RE, Schaad NW. 2004. Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol 27:755-762. http://dx.doi.org/10.1078/0723202042369884.
2. Schaad NW, Postnikova E, Lacy G, Sechler A, Agarkova I, Stromberg PE, Stromberg VK, Vidaver AK. 2006. Emended classification of xanthomonad pathogens on citrus. Syst Appl Microbiol 29:690-695. http: //dx.doi.org/10.1016/j.syapm.2006.08.001.
3. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreås L, Reysenbach AL, Smith VH, Staley JT. 2006. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102-112. http://dx.doi.org/10.1038/nrmicro1341.
4. Martinez JL, Baquero F. 2002. Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin Microbiol Rev 15:647-679. http://dx.doi.org/10.1128/CMR.15.4.647-679.2002.
5. Rosselló-Mora R, Amann R. 2001. The species concept for prokaryotes. FEMS Microbiol Rev 25:39-67. http://dx.doi.org/10.1111/j.1574-6976.2001.tb00571.x.
6. Bryant J, Chewapreecha C, Bentley SD. 2012. Developing insights into the mechanisms of evolution of bacterial pathogens from whole-genome sequences. Future Microbiol 7:1283-1296. http://dx.doi.org/10.2217/fmb.12.108.
7. Wicker E, Lefeuvre P, de Cambiaire J-C, Lemaire C, Poussier S, Prior P. 2012. Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. ISME J 6:961-974. http://dx.doi.org/10.1038/ismej.2011.160.
8. Philippe H, Douady CJ. 2003. Horizontal gene transfer and phylogenetics. Curr Opin Microbiol 6:498-505. http://dx.doi.org/10.1016/j.mib.2003.09.008.
9. Wijayawardena KB, Minchella DJ, DeWoody JA. 2013. Hosts, parasites, and horizontal gene transfer. Trends Parasitol 29:329-338. http://dx.doi.org/10.1016/j.pt.2013.05.001.
10. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J. 2005. Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733-739. http://dx.doi.org/10.1038/nrmicro1236.
11. Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A. 2008. Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200-214. http://dx.doi.org/10.1099/ijs.0.65392-0.
12. Gomez-Valero L, Rusniok C, Jarraud S, Vacherie B, Rouy Z, Barbe V, Medigue C, Etienne J, Buchrieser C. 2011. Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 12:536. http://dx.doi.org/10.1186/1471-2164 -12-536.
13. Vos M, Didelot X. 2009. A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199-208. http://dx.doi.org/10.1038 /ismej.2008.93.
14. Hayward AC. 1993. The host of Xanthomonas, p 51-54. In Swings J and Civerolo EL (ed), Xanthomonas. Springer, Dordrecht, Netherlands.
15. Stall RE, Beaulieu C, Egel DS, Hodge NC, Leite RP, Minsavage GV, Bouzar H, Jones JB, Alvarez AM, Benedict AA. 1994. Two genetically diverse groups of strains are included in Xanthomonas campestris pv. vesicatoria. Int J Syst Bacteriol 44:47-53. http://dx.doi.org/10.1099/00207713 -44-1-47.
16. Almeida NF, Yan S, Cai R, Clarke CR, Morris CE, Schaad NW, Schuenzel EL, Lacy GH, Sun X, Jones JB. 2010. PAMDB, a multilocus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 100:208-215. http://dx.doi.org/10.1094/PHYTO-100-3 -0208.
17. Jones JB, Bouzar H, Stall RE, Almira EC, Roberts PD, Bowen BW, Sudberry J, Strickler PM, Chun J. 2000. Systematic analysis of xanthomonads (Xanthomonas spp.) associated with pepper and tomato lesions. Int J Syst Evol Microbiol 50:1211-1219. http://dx.doi.org/10.1099 /00207713-50-3-1211.
18. Jones JB, Lacy GH, Bouzar H, Minsavage GV, Stall R, Schaad N. 2004. Bacterial spot-worldwide distribution, importance and review. 1st International Symposium on Tomato Diseases. Acta Hortic 695:27-33.
19. Cuppels DA, Louws FJ, Ainsworth T. 2006. Development and evaluation of PCR-based diagnostic assays for the bacterial speck and bacterial spot pathogens of tomato. Plant Dis 90:451-458. http://dx.doi.org/10.1094 /PD-90-0451.
20. Bouzar H, Jones J, Stall R, Louws F, Schneider M, Rademaker J, De Bruijn F, Jackson L. 1999. Multiphasic analysis of xanthomonads causing bacterial spot disease on tomato and pepper in the Caribbean and Central America: evidence for common lineages within and between countries. Phytopathology 89:328-335. http://dx.doi.org/10.1094/PHYTO.1999.89.4.328.
21. Bouzar H, Jones JB, Somodi GC, Stall RE, Daouzli N, Lambe RC, Felix Gastelum R, Trinidad Correa R. 1996. Diversity of Xanthomonas campestris pv. vesicatoria in tomato and pepper fields of Mexico. Can J Plant Pathol 18:75-77. http://dx.doi.org/10.1080/07060669609500659.
22. Hamza AA, Robene-Soustrade I, Jouen E, Gagnevin L, Lefeuvre P, Chiroleu F, Pruvost O. 2010. Genetic and pathological diversity among Xanthomonas strains responsible for bacterial spot on tomato and pepper in the southwest Indian Ocean region. Plant Dis 94:993-999. http://dx.doi.org/10.1094/PDIS-94-8-0993.
23. Horvath DM, Stall RE, Jones JB, Pauly MH, Vallad GE, Dahlbeck D, Staskawicz BJ, Scott JW. 2012. Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLoS One 7:e42036. http://dx.doi.org/10.1371/journal.pone.0042036.
24. Mhedbi-Hajri N, Hajri A, Boureau T, Darrasse A, Durand K, Brin C, Fischer-Le Saux M, Manceau C, Poussier S, Pruvost O. 2013. Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLoS One 8:e58474. http://dx.doi.org/10.1371/journal.pone.0058474.
25. Wichmann G, Ritchie D, Kousik CS, Bergelson J. 2005. Reduced genetic variation occurs among genes of the highly clonal plant pathogen Xanthomonas axonopodis pv. vesicatoria, including the effector gene avrBs2. Appl Environ Microbiol 71:2418-2432. http://dx.doi.org/10.1128/AEM.71.5.2418-2432.2005.
26. Parkinson N, Cowie C, Henney J, Stead D. 2009. Phylogenetic structure of Xanthomonas determined by comparison of gyrB seqeuences. Int J Syst Evol Microbiol 59:264-274. http://dx.doi.org/10.1099/ijs.0.65825-0.
27. Kebede MG, Timilsina S, Ayalew A, Admassu B, Potnis N, Minsavage GV, Goss EM, Hong JC, Strayer A, Paret M, Jones JB, Vallad GE. 2014. Molecular characterization of Xanthomonas strains responsible for bacterial spot of tomato in Ethiopia. Eur J Plant Pathol 140:677-688. http://dx.doi.org/10.1007/s10658-014-0497-3.
28. Hamza AA, Robene-Soustrade I, Jouen E, Lefeuvre P, Chiroleu F, Fisher-Le SM, Gagnevin L, Pruvost O. 2012. Multilocus sequence analysis- and amplified fragment length polymorphism-based characterization of xanthomonads associated with bacterial spot of tomato and pepper and their relatedness to Xanthomonas species. Syst Appl Microbiol 35: 183-190. http://dx.doi.org/10.1016/j.syapm.2011.12.005.
29. Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB, Ryan RP, Sharlach M, Behlau F, Dow JM, Momol MT, White FF, Preston JF, Vinatzer BA, Koebni R, Setubal JC, Norman DJ, Staskawicz BJ, Jones JB. 2011. Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12:146. http://dx.doi.org /10.1186/1471-2164-12-146.
30. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
31. Hall T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.
32. Posada D, Buckley TR. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 59:793-808. http://dx.doi.org/10.1080/10635150490522304.
33. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. http://dx.doi.org/10.1093/bioinformatics/btg180.
34. Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539-542. http://dx.doi.org/10.1093/sysbio /sys029.
35. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452. http://dx.doi.org/10.1093/bioinformatics/btp187.
36. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
37. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
38. Joseph S, Forsythe SJ. 2012. Insights into the emergent bacterial pathogen Cronobacter spp., generated by multilocus sequence typing and analysis. Front Microbiol 3:397. http://dx.doi.org/10.3389/fmicb.2012.00397.
39. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254-267. http://dx.doi.org/10.1093/molbev/msj030.
40. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463. http://dx.doi.org/10.1093/bioinformatics /btq467.
41. Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW. 2006. GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096-3098. http://dx.doi.org/10.1093/bioinformatics/btl474.
42. Didelot X, Falush D. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266. http://dx.doi.org/10.1534/genetics.106.063305.
43. Roberts MS, Cohan FM. 1993. The effect of DNA sequence divergence on sexual isolation in Bacillus. Genetics 134:401-408.
44. Posada D, Crandall KA, Holmes EC. 2002. Recombination in evolutionary genomics. Annu Rev Genet 36:75-97. http://dx.doi.org/10.1146 /annurev.genet.36.040202.111115.
45. Marcelletti S, Ferrante P, Scortichini M. 2010. Multilocus sequence typing reveals relevant genetic variation and different evolutionary dynamics among strains of Xanthomonas arboricola pv. juglandis. Diversity 2:1205-1222. http://dx.doi.org/10.3390/d2111205.
46. Obradovic A, Mavridis A, Rudolph K, Janse JD, Arsemijevic M, Jones JB, Minsavage GV, Wang JF. 2004. Characterization of PCR-based typing of Xanthomonas campestris pv. vesicatoria from peppers and tomatoes in Serbia. Eur J Plant Pathol 110:285-292. http://dx.doi.org/10.1023 /B:EJPP.0000019797.27952.1d.
47. Astua-Monge G, Minsavage GV, Stall RE, Vallejos CE, Davis MJ, Jones JB. 2000. Xv4-Avrxv4: a new gene-for-gene interaction identified between Xanthomonas campestris pv. vesicatoria race T3 and the wild tomato relative Lycopersicon pennellii. Mol Plant Microbe Interact 13:1346-1355. http://dx.doi.org/10.1094/MPMI.2000.13.12.1346.
48. Canteros BI, Minsavage GV, Jones JB, Stall RE. 1995. Diversity of plasmids in Xanthomonas campestris pv. vesicatoria. Phytopathology 85: 1482-1486. http://dx.doi.org/10.1094/Phyto-85-1482.
49. Basim H, Stall RE, Minsavage GV, Jones JB. 1999. Chromosomal gene transfer by conjugation in the plant pathogen Xanthomonas axonopodis pv. vesicatoria. Phytopathology 89:1044-1049. http://dx.doi.org/10.1094 /PHYTO.1999.89.11.1044.
50. Hert AP, Roberts PD, Momol MT, Minsavage GV, Tudor-Nelson SM, Jones JB. 2005. Relative importance of bacteriocin-like genes in antagonism of Xanthomonas perforans tomato race 3 to Xanthomonas euvesicatoria tomato race 1 strains. Appl Environ Microbiol 71:3581-3588. http: //dx.doi.org/10.1128/AEM.71.7.3581-3588.2005.
51. Jibrin MO, Timilsina S, Potnis N, Minsavage GV, Shenge KC, Akpa AD, Alegbejo MD, Vallad GE, Jones JB. 2014. First report of Xanthomonas euvesicatoria causing bacterial spot disease in pepper in northwestern Nigeria. Plant Dis http://dx.doi.org/10.1094/PDIS-06-14-0586-PDN.
52. Bui Thi Ngoc L, Vernière C, Jouen E, Ah-You N, Lefeuvre P, Chiroleu F, Gagnevin L, Pruvost O. 2010. Amplified fragment length polymorphism and multilocus sequence analysis-based genotypic relatedness among pathogenic variants of Xanthomonas citri pv. citri and Xanthomonas campestris pv. bilvae. Int J Syst Evol Microbiol 60:515-525. http://dx.doi.org/10.1099/ijs.0.009514-0.
53. Mbega ER, Wulff EG, Mabagala RB, Adriko J, Lund OS, Mortensen CN. 2012. Xanthomonads and other yellow-pigmented Xanthomonas-like bacteria associated with tomato seeds in Tanzania. Afr J Biotechnol 11: 14303-14312. http://dx.doi.org/10.5897/AJB12.1305.