Abstract
Fusarium wilt caused by Fusarium oxysporum f. sp. ciceris (Padwick) Matuo & K. Sato has become the main limiting factor for chickpea (Cicer arietinum L.) production around the world. Although the cultivation of this legume is recent in Brazil, there are reports on Fusarium spp. occurrence causing crop losses. Fourteen isolates obtained from roots of chickpea plants showing wilt and yellowing symptoms in Brazil were evaluated through phylogenetic analysis of the EF-1α region, morphological markers and pathogenicity tests. Three isolates were clustered within a distinct lineage from those already described for the FSSC. The remaining 11 isolates were clustered within the FOSC, in a different clade from F. oxysporum f. sp. ciceris. All isolates were pathogenic but showed differences in aggressiveness. Isolates of the different complexes elicited the same symptoms: yellowing, wilt and root rot of chickpea plants. Morphological markers allowed differentiating isolates from distinct complexes but not differentiating between lineages.
Similar content being viewed by others
References
Aoki T, O’Donnell K, Scandiani MM (2005) Sudden death syndrome of soybean in South America is caused by four species of Fusarium: Fusarium brasiliense sp. nov., F. cuneirostrum sp. nov., F. tucumaniae, and F. virguliforme. Mycoscience 46:162–183
Aoki T, Tanaka F, Suga H, Hyakumachi M, Scandiani MM, O’ Donnel K (2012) Fusarium azukicola sp. nov., an exotic azuki bean root-rot pathogen in Hikkaido, Japan. Mycologia 104:1068–1084
Armstrong GM, Armstrong JK (1981) Formae speciales and races of Fusarium oxysporum causing wilt diseases. In: Nelson PE, Toussoun TA, Cook RJ (eds) Fusarium: diseases, biology, and taxonomy. Pennsylvania State University Press, University Park, PA, pp 391–399
Baayen RP, O’Donnell K, Bonants PJM, Cigelnik E, Kroon LPNM, Roebroeck EJA, Waalwijk C (2000) Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nommonophyletic Formae Speciales causing wilt and rot disease. Phytophatology 90:891–900
Chand H, Khirbat SK (2009) Chickpea wilt and its management-a review. Agric Rev 30:1–12
Costa SS, Matos KS, Tessmann DJ, Seixas CDS, Pfenning LH (2016) Fusarium paranaense sp. nov., a member of the Fusarium solani species complex causes root rot on soybean in Brazil. Fungal Biol 120:51–60
Covert SF, Aoki T, O’Donnell K, Starkey D, Holliday A, Geiser DM, Cheung F, Town C, Strom A, Juba J, Scandiani M, Yang XB (2007) Sexual reproduction in the soybean sudden death syndrome pathogen Fusarium tucumaniae. Fungal Genet Biol 44:799–807
Demers JE, Garzón CD, Jiménez-Gasco MDM (2014) Striking genetic similarity races of Fusarium oxysporum f. Sp. ciceris confirms a monophyletic origin and clonal evolution of the chickpea vascular wilt pathogen. Eur J Plant Pathol 139:303–318
Di Pietro AMP, Caracuel ZM, Delgado-Jarana J, Roncero MIG (2003) Fusarium oxysporum: exploring the molecular arsenal of a vascular wilt pathogen. Mol Plant Pathol 4:315–325
Dubey SC, Priyanka K, Singh V (2014) Phylogenetic relationship between different race representative populations of Fusarium oxysporum f. Sp. ciceris in respect of translation elongation factor-1α, β-tubulin, and internal transcribed spacer region genes. Arch Microbiol 196:445–452
Gerlach W, Niremberg H (1982) The genus Fusarium: a pictorial atlas. Biologischen Bundesanstalt fur Land-und Forstwirtschaft, Berlin
Gurjar GS, Barve MP, Giri AP, Gupta VS (2009) Identification of Indian pathogenic races of Fusarium oxysporum f. Sp. ciceris with gene specific, ITS and random markers. Mycologia 101:484–495
Hepperle D (2004) SeqAssem©: a sequence analysis tool conting assembler and trace data visualization tool for molecular sequences: win32-version. Sequentx, Klein Raden
Jiménez-Díaz RM, Castillo P, Jiménez-Gasco MM, Landa BB, Navas-Cortés JA (2015) Fusarium wilt of chickpeas: biology, ecology and management. Crop Prot 73:16–27
Jiménez-Gasco MM, Milgroom MG, Jiménez-Díaz RM (2002) Gene genealogies support Fusarium oxysporum f. Sp. ciceris as a monophyletic group. Plant Pathol 51:72–77
Jiménez-Gasco MM, Navas-Cortes J, Jiménez-Díaz RM (2004) The Fusarium oxysporum f. Sp. ciceris/Cicer arietinum: a case study of the evolution of plant-pathogenic fungi into races and pathotypes. Int Microbiol 7:95–104
Jukanti AK, Gaur PM, Gowda CLL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutr 108:11–26
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing Asia, Australia
Lievens B, Rep M, Thomma BPHJ (2008) Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. Pest Manag Sci 64:781–788
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, pp. 1–8
Nalim FA, Samuels GJ, Wijesundera RL, Geiser DM (2011) New species from the Fusarium solani species complex derived from perithecia and soil in the old world tropics. Mycologia 103:1302–1330
Nene YL, Sheila YK, and Sharma SB (1996) A world list of chickpea and pigeonpea pathogens. 5th edn. Patancheru 502 324, Andhra Pradesh, India: International Crops Research Institute for the Semi-Arid Tropics. (Semi-formal publication.), 27p
Nene YL, Reddy MV, Haware MP, Ghanekar AM, Amin KS, Pande S, Sharma M (2012) Field Diagnosis of Chickpea Diseases and their Control, Information Bulletin No. 28. (revised). International Crops Research Institute for the Semi-Arid Tropics
Nirmaladevi D, Venkataramana M, Srivastava RK, Uppalapati SR, Gupta VK, Yli-Mattila T, Clement Tsui KM, Srinivas C, Niranjana SR, Chandra NS (2016) Molecular phylogeny, pathogenicity and toxigenicity of Fusarium oxysporum f.sp. lycopersici. Sci Rep 6:21367
Nylander JAA (2004) MrModeltest ver. 2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
O’Donnell K (2000) Molecular phylogeny of the Nectria haematococca–Fusarium solani species complex. Mycologia 92:919–938
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044–2049
O’Donnell K, Sutton DA, Fothergill A, Mccarthy D, Rinaldi MG, Brandt ME, Zhang N, Geiser DM (2008) Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46:2477–2490
O’Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, Van Der Lee T, Moretti A, Kang S, Kim HS, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithell S, Sutton DA, Skovgaard KR, Kistler P, Elliott HC, Davis M, Sarver MBAJ (2009) A two- locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 46:936–948
O'Donnell K, Sink S, Scandiani MM, Luque A, Colletto A, Biasoli M, Lenzi L, Salas G, González V, Ploper LD, Formento N, Pioli RN, Aoki T, Yang XB, Sarver BAJ (2010) Soybean sudden death syndrome species diversity within north and South America revealed by multilocus genotyping. Phytopathology 100:58–71
Scandiani M, Ruberti D, O’Donnell, Aoki T, Pioli R, Giorda L, Luque A, Biasoli M (2004) Recent outbreak of soybean sudden death syndrome caused by Fusarium virguliforme and F. tucumaniae in Argentina. Plant Dis 88:1044
Schroers HJ, Baayen RP, Meffert JP, Gruyter J, Hooftman M, O’Donnell K (2004) Fusarium foetens, a new species pathogenic to begonia elatior hybrids (Begonia x hiemalis) and the sister taxon of the Fusarium oxysporum species complex. Mycologia 96:393–406
Secor GA, Rivera- Varas V, Christ DS, Mathew FM, Khan MF, Varrelmann M, Bolton MD (2014) Characterization of Fusarium secorum, a new species causing Fusarium yellowing decline of sugar beet in north Central USA. Fungal Biol 118:764–775
Sharma RD, Cerkauskas RF (1985) Interação entre Meloidogyne javanica e Fusarium oxysporum f. sp. ciceris sobre o grão-de-bico. Nematol Bras 9:113–121
Silva FP, Vechiato MH, Harakava R (2014) EF-1 gene and IGS sequencing of Fusarium oxysporum f.Sp. vasinfectum and F. oxysporum f.Sp. phaseoli reveals polyphyletic origin of strains. Trop Plant Pathol 39:64–73
Smith D, Onions AHS (1994) The preservation and maintenance of living fungi. Kew: Commonwealth Mycological Institute
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Trapero-Casas A, Jiménez-Díaz RM (1985) Fungal wilt and root rot diseases of chickpea in southern Spain. Phytopathology 75:1146–1151
Westerlund FV, Campbell RN, Kimble KA (1974) Fungal root rots wilt of chickpea in California. Phytopathology 64:432–436
Wood JA, Grusak MA (2007) Nutritional value of chickpea. In: Redden RR, Chen W, Sharma B (eds) Yadav SS. CAB International, Chickpea Breeding and Management, pp 101–142
Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DM (2006) Members of the Fusarium solani species complex that cause infections in both humans and plants are common in environment. J Clin Microbiol 44:2186–2190
Acknowledgements
The first author acknowledges the financial support provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior CAPES/PNPD. Authors are grateful to Osmar Artiaga for kindly allowing collect samples in his chickpea production field. We would like to express our sincere thanks to all team members from the Laboratório de Fitopatologia-UFMG and Labroratório de Ecologia e Sistemática de Fungos-UFLA for the voluntary help. Special thanks to Edson Luis Rezende and Everson for their support and technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Olinto L. Pereira
Rights and permissions
About this article
Cite this article
Azevedo, D.M.Q., Rocha, F.S., Costa, C.A. et al. Etiology of root rot and wilt disease of chickpea in Brazil. Trop. plant pathol. 42, 273–283 (2017). https://doi.org/10.1007/s40858-017-0145-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-017-0145-5