Population typing of the causal agent of cassava bacterial blight in the Eastern Plains of Colombia using two types of molecular markers

BMC Microbiology

Adriana J Bernal²  Ralf Koebnik¹  Silvia Restrepo²  Anibal Tapiero³  César A Medina²  Lucie Poulin¹  Nathalia Arias-Rojas¹  César A Trujillo² 

[1] Institut de Recherche pour le Développement (IRD), UMR Résistance des Plantes aux Bioaggresseurs, Montpellier, France;Laboratorio de Micología y Fitopatología Uniandes (LAMFU), Universidad de Los Andes, Bogotá, Colombia;Corporación Colombiana de Investigación Agropecuaria (CORPOICA), La Libertad, Villavicencio, Colombia

关键词: Plant pathology;    Molecular markers;    Population dynamics;    Xanthomonas axonopodis pv. manihotis;   

Others  :  821426
DOI  :  10.1186/1471-2180-14-161

 received in 2013-10-08, accepted in 2014-06-10,  发布年份 2014

【 摘 要 】

Background

Molecular typing of pathogen populations is an important tool for the development of effective strategies for disease control. Diverse molecular markers have been used to characterize populations of Xanthomonas axonopodis pv. manihotis (Xam), the main bacterial pathogen of cassava. Recently, diversity and population dynamics of Xam in the Colombian Caribbean coast were estimated using AFLPs, where populations were found to be dynamic, diverse and with haplotypes unstable across time. Aiming to examine the current state of pathogen populations located in the Colombian Eastern Plains, we also used AFLP markers and we evaluated the usefulness of Variable Number Tandem Repeats (VNTRs) as new molecular markers for the study of Xam populations.

Results

The population analyses showed that AFLP and VNTR provide a detailed and congruent description of Xam populations from the Colombian Eastern Plains. These two typing strategies clearly separated strains from the Colombian Eastern Plains into distinct populations probably because of geographical distance. Although the majority of analyses were congruent between typing markers, fewer VNTRs were needed to detect a higher number of genetic populations of the pathogen as well as a higher genetic flow among sampled locations than those detected by AFLPs.

Conclusions

This study shows the advantages of VNTRs over AFLPs in the surveillance of pathogen populations and suggests the implementation of VNTRs in studies that involve large numbers of Xam isolates in order to obtain a more detailed overview of the pathogen to improve the strategies for disease control.

【 授权许可】

   
2014 Trujillo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Lannou C, Hubert P, Gimeno C: Competition and interactions among stripe rust pathotypes in wheat-cultivar mixtures. Plant Pathol 2005, 54(5):699-712.
• [2]Mundt CC: Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 2002, 40:381-410.
• [3]McDonald BA, Linde C: Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 2002, 40:349-379.
• [4]Stukenbrock EH, McDonald BA: The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 2008, 46:75-100.
• [5]Barrett LG, Thrall PH, Burdon JJ, Linde CC: Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 2008, 23(12):678-685.
• [6]Maraite H: Xanthomonas campestris pathovars on cassava: cause of bacterial blight and bacterial necrosis. In Xanthomonas. Edited by Swings JG, Civerolo EL. London: Chapman and Hall; 1993:18-24.
• [7]Lozano J: Cassava bacterial blight: a manageable disease. Plant Dis 1986, 70:1089-1093.
• [8]Restrepo S, Velez CM, Duque MC, Verdier V: Genetic structure and population dynamics of Xanthomonas axonopodis pv. manihotis in Colombia from 1995 to 1999. Appl Environ Microb 2004, 70(1):255-261.
• [9]Restrepo S, Velez CM, Verdier V: Measuring the genetic diversity of Xanthomonas axonopodis pv. manihotis within different fields in Colombia. Phytopathology 2000, 90(7):683-690.
• [10]Ogunjobi AA, Fagade OE, Dixon AG: Comparative analysis of genetic variation among Xanthomonas axonopodis pv manihotis isolated from the western states of Nigeria using RAPD and AFLP. Indian J Microbiol 2010, 50(2):132-138.
• [11]Verdier V, Boher B, Maraite H, Geiger JP: Pathological and molecular characterization of Xanthomonas campestris isolates causing diseases of cassava (Manihot esculenta). Appl Environ Microb 1994, 60:4478-4486.
• [12]Verdier V, Dongo P, Boher B: Assessment of genetic diversity among strains of Xanthomonas campestris pv manihotis. J Gen Microbiol 1993, 139:2591-2601.
• [13]Verdier V, Restrepo S, Mosquera G, Duque MC, Gerstl A, Laberry R: Genetic and pathogenic variation of Xanthomonas axonopodis pv. manihotis in Venezuela. Plant Pathol 1998, 47:601-608.
• [14]Restrepo S, Verdier V: Geographical differentiation of the population of Xanthomonas axonopodis pv. manihotis in Colombia. Appl Environ Microb 1997, 63(11):4427-4434.
• [15]Trujillo CA, Ochoa JC, Mideros MF, Restepo S, López C, Bernal A: A complex population structure of the Cassava Pathogen Xanthomonas axonopodis pv. manihotis in recent years in the Caribbean Region of Colombia. Microb Ecol 2014., 67(4) doi:10.1007/s00248-014-0411-8
• [16]Restrepo S, Du que M, Tohme J, Verdier V: AFLP fingerprinting: an efficient technique for detecting genetic variation of Xanthomonas axonopodis pv. manihotis. Microbiology 1999, 145(Pt 1):107-114.
• [17]Fillo S, Giordani F, Anniballi F, Gorge O, Ramisse V, Vergnaud G, Riehm JM, Scholz HC, Splettstoesser WD, Kieboom J, Olsen JS, Fenicia L, Lista F: Clostridium botulinum group I strain genotyping by 15-locus multilocus variable-number tandem-repeat analysis. J Clin Microbiol 2011, 49(12):4252-4263.
• [18]Blears MJ, De Grandis SA, Lee H, Trevors JT: Amplified fragment length polymorphism (AFLP): a review of the procedure and its applications. J Ind Microbiol Biot 1998, 21:99-114.
• [19]Chiou CS: Multilocus variable-number tandem repeat analysis as a molecular tool for subtyping and phylogenetic analysis of bacterial pathogens. Expert Rev Mol Diagn 2010, 10(1):5-7.
• [20]Garcia-Yoldi D, Le Fleche P, De Miguel MJ, Munoz PM, Blasco JM, Cvetnic Z, Marin CM, Vergnaud G, Lopez-Goni I: Comparison of multiple-locus variable-number tandem-repeat analysis with other PCR-based methods for typing Brucella suis isolates. J Clin Microbiol 2007, 45(12):4070-4072.
• [21]Van Belkum A: Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol Med Mic 2007, 49(1):22-27.
• [22]Mazars E, Lesjean S, Banuls AL, Gilbert M, Vincent V, Gicquel B, Tibayrenc M, Locht C, Supply P: High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc Natl Acad Sci U S A 2001, 98(4):1901-1906.
• [23]Roring S, Scott A, Brittain D, Walker I, Hewinson G, Neill S, Skuce R: Development of variable-number tandem repeat typing of Mycobacterium bovis: comparison of results with those obtained by using existing exact tandem repeats and spoligotyping. J Clin Microbiol 2002, 40(6):2126-2133.
• [24]Keim P, Price LB, Klevytska AM, Smith KL, Schupp JM, Okinaka R, Jackson PJ, Hugh-Jones ME: Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J Bacteriol 2000, 182(10):2928-2936.
• [25]Melles DC, Schouls L, Francois P, Herzig S, Verbrugh HA, van Belkum A, Schrenzel J: High-throughput typing of Staphylococcus aureus by amplified fragment length polymorphism (AFLP) or multi-locus variable number of tandem repeat analysis (MLVA) reveals consistent strain relatedness. Eur J Clin Microbiol Infect Dis 2009, 28(1):39-45.
• [26]Coletta-Filho HD, Takita MA, de Souza AA, Aguilar-Vildoso CI, Machado MA: Differentiation of strains of Xylella fastidiosa by a variable number of tandem repeat analysis. Appl Environ Microb 2001, 67(9):4091-4095.
• [27]Ngoc LB, Verniere C, Vital K, Guerin F, Gagnevin L, Brisse S, Ah-You N, Pruvost O: Development of 14 minisatellite markers for the citrus canker bacterium, Xanthomonas citri pv. citri. Mol Ecol Resour 2009, 9(1):125-127.
• [28]N’Guessan CA, Brisse S, Le Roux-Nio AC, Poussier S, Kone D, Wicker E: Development of variable number of tandem repeats typing schemes for Ralstonia solanacearum, the agent of bacterial wilt, banana Moko disease and potato brown rot. J Microbiol Meth 2013, 92(3):366-374.
• [29]Zhao S, Poulin L, Rodriguez RL, Serna NF, Liu SY, Wonni I, Szurek B, Verdier V, Leach JE, He YQ, Feng JX, Koebnik R: Development of a variable number of tandem repeats typing scheme for the bacterial rice pathogen Xanthomonas oryzae pv. oryzicola. Phytopathology 2012, 102(10):948-956.
• [30]Stevenson K, Alvarez J, Bakker D, Biet F, de Juan L, Denham S, Dimareli Z, Dohmann K, Gerlach GF, Heron I, Kopecna M, May L, Pavlik I, Sharp JM, Thibault VC, Willemsen P, Zadoks RN, Greig A: Occurrence of Mycobacterium avium subspecies paratuberculosis across host species and European countries with evidence for transmission between wildlife and domestic ruminants. BMC Microbiol 2009, 9:212.
• [31]Pourcel C, Visca P, Afshar B, D’Arezzo S, Vergnaud G, Fry NK: Identification of variable-number tandem-repeat (VNTR) sequences in Legionella pneumophila and development of an optimized multiple-locus VNTR analysis typing scheme. J Clin Microbiol 2007, 45(4):1190-1199.
• [32]Castiblanco LF, Gil J, Rojas A, Osorio D, Gutierrez S, Munoz-Bodnar A, Perez-Quintero AL, Koebnik R, Szurek B, Lopez C, Restrepo S, Verdier V, Bernal AJ: TALE1 from Xanthomonas axonopodis pv. manihotis acts as a transcriptional activator in plant cells and is important for pathogenicity in cassava plants. Mol Plant Pathol 2013, 14(1):84-95.
• [33]Verdier V, Mosquera G, Assigbétsé K: Detection of the Cassava bacterial blight pathogen, Xanthomonas axonopodis pv. manihotis, by Polymerase chain reaction. Plant Dis 1998, 82(1):79-83.
• [34]Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M: AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 1995, 23(21):4407-4414.
• [35]Hunter PR, Gaston MA: Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 1988, 26(11):2465-2466.
• [36]Arrieta-Ortiz ML, Rodriguez-R LM, Pérez AL, Poulin L, Díaz AC, Arias Rojas N, Trujillo C, Restrepo-Benavides M, Bart R, Boch J, Boureau T, Darrasse A, David P, Bernonville TD, Fontanilla P, Gagnevin L, Guérin F, Jacques MA, Lauber E, Lefeuvre P, Medina C, Medina E, Montenegro N, Muñoz-Bodnar A, Noël L, Ortiz-Quiñones JF, Osorio D, Pardo C, Patil PB, Poussier S, et al.: Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. manihotis strain CIO151. PLoS One 2013, 8(11):e79704.
• [37]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [38]Peakall R, Smouse PE: GenAlEx 6.5: genetic analysis in Excel: population genetic software for teaching and research--an update. Bioinformatics 2012, 28(19):2537-2539.
• [39]Meirmans PG, Van-Tienderen PH: GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 2004, 4:792-794.
• [40]Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23(2):254-267.
• [41]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155(2):945-959.
• [42]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14(8):2611-2620.
• [43]Wright S: Genetical structure of populations. Nature 1950, 166(4215):247-249.
• [44]Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RG: Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 1996, 9(5):745-753.
• [45]Levinson G, Gutman GA: Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 1987, 4(3):203-221.
• [46]Torres-Cruz J, van der Woude MW: Slipped-strand mispairing can function as a phase variation mechanism in Escherichia coli. J Bacteriol 2003, 185(23):6990-6994.
• [47]Comas I, Homolka S, Niemann S, Gagneux S: Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS One 2009, 4(11):e7815.
• [48]Aguilera Díaz M: La yuca en el Caribe colombiano: De cultivo ancestral a agroindustrial. Documentos de trabajo sobre economía regionalhttp://www.banrep.gov.co/sites/default/files/publicaciones/archivos/dtser_158.pdf: webcite Banco de la República de Colombia 2012
• [49]Lindstedt BA: Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis 2005, 26(13):2567-2582.
• [50]Ramisse V, Houssu P, Hernandez E, Denoeud F, Hilaire V, Lisanti O, Ramisse F, Cavallo JD, Vergnaud G: Variable number of tandem repeats in Salmonella enterica subsp. enterica for typing purposes. J Clin Microbiol 2004, 42(12):5722-5730.
• [51]Chang CH, Chang YC, Underwood A, Chiou CS, Kao CY: VNTRDB: a bacterial variable number tandem repeat locus database. Nucleic Acids Res 2007, 35(Database issue):D416-D421.
• [52]Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M, Petriello A, Krasileva K, Dahlbeck D, Medina C, Alicai T, Kumar L, Moreira LM, Rodrigues-Neto J, Verdier V, Santana MA, Kositcharoenkul N, Vanderschuren H, Gruissem W, Bernal A, Staskawicz BJ: High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc Natl Acad Sci U S A 2012, 109(28):E1972-E1979.