Abstract
Plant pathogenic Xanthomonas species attack a wide range of agriculture crops and is capable of surviving on weeds. In this study, Xanthomonas strains obtained from weeds grown withing vegetable crop fields in the state of Pernambuco, Northeast Brazil, were identified. Bacterial colonies resembling Xanthomonas were obtained from Aeollanthus suaveolens (strain CCRMXe03), Amaranthus lividus (CCRMXe01 and CCRMXe02), Sida glomerata (CCRMXe04), and Emilia fosbergii (CCRMXe04). All weeds but E. fosbergii exhibited lesions on the leaves. Phylogenetic analysis of the gyrB and rpoD genes and PCR-specific assays allowed to identify X. euvesicatoria pv. euvesicatoria (CCRMXe01, CCRMXe02, CCRMXe03, and CCRMXe04) and X. campestris pv. campestris (CCRMXcc371). All strains but CCRMXe03 were pathogenic to its host of origin. All X. euvesicatoria pv. euvesicatoria strains were pathogenic to leaves and fruits of tomato and bell pepper. Two strains, CCRMXe03 and CCRMXe04, were capable of inducing soft rot in fruits. Amylolytic activity was found in all strains and two strains (CCRMXe03 and CCRMXe04) degraded pectate. Strain CCRMXcc371 was pathogenic to cabbage, kale, cauliflower, and broccoli. This work provides new knowledge of hosts for two important plant pathogenic bacteria for vegetable crops.
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References
Adriko J, Mbega ER, Mortesen CN, Wulff EG, Tushemereirwe WK, Kubiriba J, Lund OS (2014) Improved PCR for identification of members of the genus Xanthomonas. European Journal of Plant Pathology 138:293–306
Araújo ER, Costa JR, Pontes NC, Quezado-Duval AM (2015) Xanthomonas perforans and X. gardneri associated with bacterial leaf spot on weeds in Brazilian tomato fields. European Journal of Plant Pathology 143:543–548
Bila J, Mondjana AM, Mortensen CN, Lund OS (2012) Podridão negra de repolho em Moçambique: estratégias para o manejo sustentável da doença. Dinamarca DSHC, Copenhagen
Bradbury JF (1993) Guide of plant pathogenic bacteria. C.A.B. International, Slough
Chaves ALR, Braun MR, Eiras M, Colariccio A, Galleti SR (2003) Erigon bonariensis: hospedeira alternativa do Lettuce mosaic virus no Brasil. Fitopatologia Brasileira 28:307–311
Constantin EC, Cleenwerck I, Maes M, Baeyen S, Van Malderghem C, Vos PDE, Cottyn B (2016) Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathology 65:792–806
Costa JR, Araújo ER, Becker WF, Ferreira MASV, Quezado-Duval AM (2012) Ocorrência e caracterização do complexo de espécies causadoras da mancha bacteriana do tomateiro no Alto Vale do Rio do Peixe, SC. Tropical Plant Pathology 37:149–154
Cuppels D, Kelman A (1974) Evaluation of selective media for isolation of soft-rot bacteria from soil and plant tissue. Phytopathology 64:468–475
EPPO - European and Mediterranean Plant Protection Organization (2013) Xanthomonas spp. (Xanthomonas euvesicatoria, Xanthomonas gardneri, Xanthomonas perforans, Xanthomonas vesicatoria), causing bacterial spot of tomato and sweet pepper. EPPO Bulletin 43:7–20
Fargier E, Saux MF, Manceau CA (2011) Multilocus sequence analysis of Xanthomonas campestris reveals a complex structure within crucifer-attacking pathovars of this species. Systematic Applied Microbiology 34:156–165
Gama MAS, Mariano RLR, Silva Júnior WJ, Farias ARG, Barbosa MAG, Ferreira MASV, Costa Júnior CRL, Santos LA, Souza EB (2018) Taxonomic repositioning of Xanthomonas campestris pv. viticola (Nayudu 1972) Dye 1978 as Xanthomonas citri pv. viticola (Nayudu 1972) Dye 1978 comb. nov. and emendation of the description of Xanthomonas citri pv. anacardii to include pigmented isolates pathogenic to cashew plant. Phytopathology 108:1143–1153
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Hamza AA, Robène-Soustrade I, Boyer C, Laurent A, Jouen E, Wicker E, Prior P, Pruvost O (2010) A new type of strain of Xanthomonas euvesicatoria causing bacterial spot of tomato and pepper in Grenada. Disease Notes 94:1264
Hauben L, Vauterin L, Swings J, Moore ERB (1997) Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. International Journal of Systematic Bacteriology 47:328–335
He Y-Q, Zhang L, Jiang B-L, Zhang Z-C, Xu R-K, Tang D-J, Qin J, Jiang W, Zhang X, Liao J, Cao J-R, Zhang S-S, Wei M-L, Liang X-X, Lu G, Feng J-X, Chen B, Cheng J, Tang J-L (2007) Comparative and functional genomics reveals genetic diversity and determinants of host specificity among reference strains and a large collection of Chinese isolates of the phytopathogen Xanthomonas campestris pv. campestris. Genome Biology 8:R218. https://doi.org/10.1186/gb-2007-8-10-r218
Ignatov A, Sechler A, Schuenzel EL, Agarkova I, Oliver B, Vidaver AK, Schaad NW (2007) Genetic diversity in populations of Xanthomonas campestris pv. campestris in cruciferous weeds in Central Coastal California. Phytopathology 97:803–812
Jensen BD, Vicente JG, Manandhar HK, Roberts SJ (2010) Occurrence and diversity of Xanthomonas campestris pv. campestris in vegetable Brassica fields in Nepal. Plant Disease 94:298–305
Jones JB, Pohronezny KL, Stall RE, Jones JP (1986) Survival of Xanthomonas campestris pv. vesicatoria in Florida on crop residue, weeds, seeds, and volunteer tomato plants. Phytopathology 76:430–434
Jones JB, Lacy GH, Bouzar H, Stall RE, Schaad NW (2004) Reclassification of the Xanthomonas associated with bacterial spot disease of tomato and pepper. Systematic and Applied Microbiology 27:755–762
Kado EI, Heskett MG (1970) Seletive media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas and Xanthomonas. Phytopathology 60:969–976
Karam D, Melhorança AL, Oliveira MF, Silva JAA (2010) Cultivo do milho: Plantas daninhas. Embrapa Milho e Sorgo. Sistema de Produção, versão eletrônica, 6° ed. Available at: http://www.cnpms.embrapa.br/publicacoes/milho_6_ed/plantasdaninhas.html. Accessed on 18 Jul 2019
Karavina C, Mandumbu R, Parwada C, Zivenge E (2011) Epiphytic Survival of Xanthomonas axonopodis pv. phaseoli. Journal of Animal Plant Sciences 9:1161–1168
Kishun R, Chand R (1988) Epiphytic survival of Xanthomonas campestris pv. campestris on Centella asiatica (L.) Urban. International Journal of Tropical Plant Diseases 6:189–193
Koenraadt H, Van Betteray B, Germain R, Hiddink G, Jones JB, Oosterhof J, Rijlaarsdam A, Roorda P, Wouldt B (2009) Development of specific primers for the molecular detection of bacterial spot of pepper and tomato. Acta Hort 808:99–102
Krauthausen HJ, Laun N, Wohanka W (2011) Methods to reduce the spread of the black rot pathogen, Xanthomonas campestris pv. campestris, in brassica transplants. Journal of Plant Diseases and Protection 118:7–16
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology Evolution 33:1870–1874
Kurozawa C, Pavan MA (2005) Doenças do tomateiro (Lycopersicon esculentum Mill). In: Kimati H, Amorim L, Rezende JAM, Bergamin Filho A, Camargo LEA (Eds.) Manual de fitopatologia: doenças das plantas cultivadas: Editora Ceres, São Paulo. pp. 607–626
Kyeon M-S, Son S-H, Noh Y-H, Kim Y-E, Lee H-I, Cha J-S (2016) Xanthomonas euvesicatoria causes bacterial spot disease on pepper plant in Korea. Plant Pathology Journal 32:431–440
Leu YS, Deng WL, Yang WS, Wu YF, Cheng AS, Hsu ST, Tzeng KC (2010) Multiplex polymerase chain reaction for simultaneous detection of Xanthomonas campestris pv. campestris and X. campestris pv. raphani. Plant Pathology Bulletin 19:137–147
Mileo LJ, Bentes JLS, Silva JF, Christoffoleti PJ (2006) Plantas de cobertura de solo como hospedeiras alternativas de Colletotrichum guaranicola. Planta Daninha 24:677–683
Mileo LJ, Silva JF, Bentes JLS, Christoffoleti PJ (2007) Plantas daninhas hospedeiras alternativas de Colletotrichum guaranicola em cultivos de guaraná no estado do Amazonas. Planta Daninha 25:771–782
Mirik M, Selcuk F, Aysan Y, Sahin F (2008) First outbreak of bacterial black rot on cabbage, broccoli, and brussels sprouts caused by Xanthomonas campestris pv. campestris in the Mediterranean Region of Turkey. Plant Disease 92:176–176
Nylander J (2004) MrModeltest V2. Program Distributed by the Author. Uppsala University, Evolutionary Biology Centre
Palacio-Bielsa A, Cambra MA, López MM (2009) PCR detection and identification of plant-pathogenic bacteria: updated review of protocols (1989–2007). Journal of Plant Pathology 91:249–297
Pan Y-B, Grisham MP, Burner DM, Legendre BL, Wei Q (1999) Development of polymerase chain reaction primers highly specific for Xanthomonas albilineans, the causal bacterium of sugarcane leaf scald disease. Plant Disease 83:218–222
Park DS, Hyun JW, Park YJ, Kim JS, Kang HW, Hahn JH, Go SJ (2006) Sensitive and specific detection of Xanthomonas axonopodis pv. citri by PCR using pathovar specific primers based on hrpW gene sequences. Microbiological Research 161:145–149
Pereira RC, Araújo ER, Ferreira MASV, Quezado-Duval AM (2011) Occurrence of Xanthomonas species causing bacterial spot in fresh market tomato fields in Brazil. Acta Horticulturae 914:61–64
Peruch LAM, Michereff SJ, Araújo IB (2006) Levantamento da intensidade da alternariose e podridão negra em cultivos orgânicos de brássicas em Pernambuco e Santa Catarina. Horticultura Brasileira 24:464–469
Popović T, Balaž J, Starović M, Trkulja N, Ivanović Ž, Ignjatov M, Jošić D (2013) First report of Xanthomonas campestris pv. campestris as the causal agent of black rot on oilseed rape (Brassica napus) in Serbia. Plant Disease 97:418–418
Potnis N, Timilsina S, Strayer A, Shantharaj D, Barak JD, Paret ML, Vallad GE, Jones JB (2015) Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Molecular Plant Pathology 16:907–920
Pusey PL, Wilson CL (1984) Postharvest biological control of stone fruit brown rot by Bacillus subtilis. Plant Disease 68:753–756
Quezado-Duval AM, Lopes CA, Leite Júnior RP, Lima MF, Camargo LEA (2005) Diversity of Xanthomonas spp. associated with bacterial spot of processing tomatoes in Brazil. Acta Horticulturae 695:101–108
Quezado-Duval AM, Lopes CA (2010) Mancha bacteriana: uma atualização para o sistema de produção integrada de tomate indústria. Embrapa Hortaliças, Brasília (Circular Técnica 84)
Rathaur PS, Singh D, Raghuwanshi R, Yadava DK (2015) Pathogenic and genetic characterization of Xanthomonas campestris pv. campestris races based on Rep-PCR and Multilocus Sequence Analysis. Journal of Plant Pathology Microbiology 6:1000317. https://doi.org/10.4172/2157-7471.1000317
Rodrigues Neto J, Malavolta Júnior VA (1995) Doenças causadas por bactérias em crucíferas. Informe Agropecuário 17:56–59
Rodriguez-R LM, Grajales A, Arrieta-Ortiz ML, Salazar C, Restrepo S, Bernal A (2012) Genomes-based phylogeny of the genus Xanthomonas. BMC Microbiology 12. https://doi.org/10.1186/1471-2180-12-43
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Schaad NW, Dianese JC (1981) Cruciferous weeds as sources of inoculum of Xanthomonas campestris in black rot of crucifers. Phytopathology 71:1215–1220
Silva AC, Ferreira FA, Ferreira LR (2006) Manejo integrado de plantas daninhas em hortaliças. Pesquisa Tecnologia 3:1–7
Silva JC, Silva Júnior TAF, Soman JM, Tomasin TD, Sartori MP, Maringoni AC (2017) Survival of Xanthomonas campestris pv. campestris in the phyllosphere and rhizosphere of weeds. Plant Pathology 19:1517–1526
Singh D, Rathaur PS, Vicente JG (2016) Characterization, genetic diversity and distribution of Xanthomonas campestris pv. campestris races causing black rot disease in cruciferous crops of India. Plant Pathology 65:1411–1418
Staden R, Beal KF, Bolfield JK (1998) The Staden Package. Bioinformatic Method Protocol 132:115–130
Stall RE, Beaulieu C, Egel D, 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. International Journal of Systematic Bacteriology 44:47–53
Tayi L, Maku RV, Patel HK, Sonti RV (2016) Identification of pectin degrading enzymes secreted by Xanthomonas oryzae pv. oryzae and determination of their role in virulence on rice. PLoS ONE 11:e0166396
Vauterin L, Hoste B, Kersters K, Swings J (1995) Reclassification of Xanthomonas. International Journal of Systematic Bacteriol 45:472–489
Young JM, Park CD, Shearman HM, Fargier E (2008) A multilocus sequence analysis of the genus Xanthomonas. Systematic and Applied Microbiology 31:366–377
Acknowledgements
This study was financed in part by The Brazilian National Council for Scientific and Technological Development (CNPq), with a scholarship granted to LVSS, the Coordination for the Improvement of Higher Education Personnel (CAPES) - Finance Code 001 (Proc. No. 23038.003635/2013-60) and by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), with a research grant to KCSF (AUXPE 1585/2013).
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LVSS, EAM, KCFS and AMFS planed, designed, executed experimental work, conducted data analyses and wrote the manuscript, AMQD and GMRA, conducted data analyses and wrote the manuscript, and MASG and EBS planed, designed and wrote the manuscript.
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Santos, L.V.S., Melo, E.A., Silva, A.M.F. et al. Weeds as alternate hosts of Xanthomonas euvesicatoria pv. euvesicatoria and X. campestris pv. campestris in vegetable-growing fields in the state of Pernambuco, Brazil. Trop. plant pathol. 45, 484–492 (2020). https://doi.org/10.1007/s40858-020-00350-z
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DOI: https://doi.org/10.1007/s40858-020-00350-z