Abstract
A framework genetic map was developed for the fungal pathogen Colletotrichum lindemuthianum, the causal agent of anthracnose of common bean (Phaseolus vulgaris L.). This is the first genetic map for any species within the family Melanconiaceae and the genus Colletotrichum and provides the first estimate of genome length for C. lindemuthianum. The map was generated using 106 haploid F1 progeny derived from crossing two Mexican C. lindemuthianum isolates differing in two avirulence genes (AvrclMex and AvrclTO). The map comprises 165 AFLP markers covering 1,897 cM with an average spacing of 11.49 cM. The markers are distributed over 19 major linkage groups containing between 5 and 25 markers each and the genome length was estimated to be approximately 3,241 cM. The avirulence genes AvrclMex and AvrclTO segregate in a 1:1 ratio supporting the gene for gene hypothesis for the incompatible reaction between C. lindemuthianum and P. vulgaris, but could not be incorporated into the genetic map. This initial outline map forms the basis for the development of a more detailed C. lindemuthianum linkage map, which would include other types of molecular markers and allow the location of genes previously isolated and characterized in this species.
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References
Bryson RJ (1990) Sexual hybridization and the genetics of pathogenic specificity in Colletotrichum lindemuthianum. Ph.D. Thesis, University of Birmingham
Bryson RJ, Caten CE, Holloman DW, Bailey JA (1992) Sexuality and genetics of Colletotrichum. In: Bailey JA, Jeger MJ (eds) Colletotrichum: biology, pathology and control. CAB International, Wallingford, pp 27–46
Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182
Cozijnsen AJ, Popa KM, Purwantara A, Rolls BD, Howlett BJ (2000) Genome analysis of the plant pathogenic ascomycete Leptosphaeria maculans; mapping mating type and host specificity loci. Mol Plant Pathol 1:293–302
Dioh W, Tharreau D, Notteghem JL, Orbach M, Lebrun MH (2000) Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant Microbe Interact 13:217–227
Farman ML, Eto Y, Nakao T, Tosa Y, Nakayashiki H, Mayama S, Leong SA (2002) Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol Plant Microbe Interact 15:6–16
Farman ML, Leong SA (1998) Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: discrepancy between the physical and genetic maps. Genetics 150:1049–1058
Flor HH (1971) Current status of gene-for-gene concept. Annu Rev Phytopathol 9:275–296
Forche A, Xu J, Vilgalys R, Mitchell TG (2000) Development and characterization of a genetic linkage map of Cryptococcus neoformans var. neoformans using amplified fragment length polymorphisms and other markers. Fungal Genet Biol 31:189–203
González M, Rodríguez R, Zavala ME, Jacobo JL, Hernández F, Acosta J, Martínez O, Simpson J (1998) Characterization of Mexican isolates of Colletotrichum lindemuthianum by using differential cultivars and molecular markers. Phytopathology 88:292–299
González-Chavira M, Rodríguez-Guerra R, Hernández-Godínez F, Acosta-Gallegos JA, Martínez de la Vega O, Simpson J (2004) Analysis of pathotypes of Colletotrichum lindemuthianum found in the central region of Mexico and resistance in elite germ plasm of Phaseolus vulgaris. Plant Dis 88:152–156
Gout L, Fudal I, Kuhn M-L, Blaise F, Eckert M, Cattolico L, Balesdent M-H, Rouxel T (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60:67–80
Hulbert SH, Ilott TW, Legg EJ, Lincoln SE, Lander ES, Michelmore RW (1988) Genetic analysis of the fungus, Bremia lactucae, using restriction fragment length polymorphisms. Genetics 120:947–958
Jurgenson JE, Bowden RL, Zeller KA, Leslie JF, Alexander NJ, Plattner RD (2002a) A genetic map of Gibberella zeae (Fusarium graminearum). Genetics 160:1451–1460
Jurgenson JE, Zeller KA, Leslie JF (2002b) Expanded genetic map of Gibberella moniliformis (Fusarium verticillioides). Appl Environ Microbiol 68:1972–1979
Kang S, Sweigard JA, Valent B (1995) The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 8:939–948
Kelly JD, Vallejo VA (2004) A comprehensive review of the major genes conditioning resistance to anthracnose in common bean. HortScience 39:1196–1207
Kema GHJ, Goodwin SF, Hamza S, Vestasppen ECP, Cavaletto JR, Van Der Lee TAJ, de Weerdt M, Bonants PJM, Waalwijk C (2002) A combined amplified fragment length polymorphism and randomly amplified polymorphism DNA genetic linkage map of Mycosphaerella graminicola, the Septoria tritici leaf blotch pathogen of wheat. Genetics 161:1497–1505
Kerrigan RW, Royer JC, Baller LM, Hohli Y, Horgen PA, Anderson JB (1993) Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics 13:225–236
Kimati H, Galli F (1970) Glomerella cingulata (Stonem) Spauld et Schrenk f.sp. phaseoli, fase ascogena do agente causal da anthracnose do feijoeiro. Anais da Escola Superior de Agricultura “Luiz de Quieroz” 27:411–437
Knogge W (1996) Fungal infection of plants. Plant Cell 8:1711–1722
Latunde-Dada AO (2001) Colletotrichum: tales of forcible entry, stealth, transient confinement and breakout. Mol Plant Pathol 2:187–198
Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 24:842–845
Laugé R, De Wit PJGM (1998) Fungal avirulence genes: structure and possible functions. Fungal Genet Biol 24:285–297
Leach JE, Cruz CMV, Bai J, Leung H (2001) Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu Rev Phytopathol 39:187–224
Lenné JM (1992) Colletotrichum diseases of legumes. In: Bailey JA, Jeger MJ (eds) Colletotrichum: biology, pathology and control. CAB International, Wallingford, pp 134–166
Lichtenzveig J, Winter P, Abbo S, Shtienberg D, Kaiser WJ, Kahl G (2002) Towards the firs linkage map of the Didymella rabiei genome. Phytoparasitica 30:467–472
Lind M, Olson A, Stenlid J (2005) An AFLP-markers based genetic linkage map of Heterobasidion annosum locating intersterility genes. Fungal Genet Biol 42:519–527
Linning R, Lin D, Lee N, Abdennadher M, Gaudet D, Thomas P, Mills D, Kronstad JW, Bakkeren G (2004) Marker-based cloning of the region containing the UhAvr1 avirulence gene from the basidiomycete barley pathogen Ustilago hordei. Genetics 166:99–111
Kubisiak TL, Milgroom MG (2006) Markers linked to vegetative incompatibility (vic) genes and a region of high heterogeneity and reduced recombination near the mating type locus (MAT) in Cryphonectria parasitica. Fungal Genet Biol 43:453–463
Masel AM, Irwin JAG, Manners JM (1993a) DNA addition or deletion is associated with a major karyotype polymorphism in the fungal phytopathogen Colletotrichum gloeosporioides. Mol Gen Genet 237:73–80
Masel AM, Irwin JAG, Manners JM (1993b) Minichromosomes of Colletotrichum sp. infecting several host species in various countries. Mycol Res 97:852–856
Michelmore RW, Paran I, Kesseli V (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88:9828–9832
O’Sullivan D, Tosi P, Creusot F, Cooke M, Phan T-H, Dron M, Langin T (1998) Variation in genome organization of the plant pathogenic fungus Colletotrichum lindemuthianum. Curr Genet 33:291–298
Pastor-Corrales MA (1991) Estandarización de variedades diferenciales y de asignación de razas de Colletotrichum lindemuthianum. (Abstr.) Phytopathology 81:694
Pedersen C, Rasmussen SW, Giese H (2002) A genetic map of Blumeria graminis based on functional genes, avirulence genes, and molecular markers. Fungal Genet Biol 35:235–246
Perfect SE, Hunghes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal–plant interactions. Fungal Genet Biol 27:186–198
Phan HTT, Ford R, Taylor PWJ (2003) Mapping the mating type locus of Ascochyta rabiei, the causal agent of ascochyta blight of chickpea. Mol Plant Pathol 4:373–381
Pongam P, Osborn TC, Williams PH (1998) Genetic analysis and identification of amplified fragment length polymorphism markers linked to the alm1 avirulence gene of Leptosphaeria maculans. Phytopathology 88:1068–1072
Remington DL, Whetten RW, Liu B-H, O’Malley DM (1999) Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor Appl Genet 98:1279–1292
Rodríguez-Guerra R, Ramírez-Rueda M-T, Simpson J (2004) Capacidad de anastomosis de cepas del hongo Colletotrichum lindemuthianum (Sacc. et Magn.) Scrib., agente causal de la antracnosis del frijol (Phaseolus vulgaris L.). Rev Mex Fitopatol 22:37–43
Rodríguez-Guerra R, Ramírez-Rueda M-T, Cabral-Enciso M, García-Serrano M, Lira-Maldonado Z, González-Chavira M, Simpson J (2005) Heterothallic mating observed between Mexican isolates of Glomerella lindemuthiana. Mycologia 97:793–803
Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B (1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the RrS1 resistance genotype. EMBO J 14:4168–4177
Sierotzki H, Gessler C (1998) Analysis of a cross of two Venturia inaequalis strains that differ in virulence. J Phytopathol 146:515–519
Shear CL, Wood AK (1913) Studies of fungus parasites belonging to the genus Glomerella. U.S.D.A. Bur Pl Industry Bull 252:1–110
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744
Swart K (1996) Mapping and breeding strategies. In: Bos CJ (ed) Fungal genetics principles and practice, pp 295–315
Sweigard JA, Carroll AM, Kang S, Farral L, Chumley FG, Valent B (1995) Identification, cloning, and characterization of PWL2, a gene for host species-specificity in the rice blast fungus. Plant Cell 7:1221–1233
Tu JC (1985) An improved Mathur’s medium for growth, sporulation, and germination of spores of Colletotrichum lindemuthianum. Microbios 44:87–93
Tu JC (1992) Colletotrichum lindemuthianum on bean: population dynamics of the pathogen and breeding for resistance. In: Bailey JA, Jeger MJ (eds) Colletotrichum: biology, pathology and control. CAB International, Wallingford, pp 203–224
Tzeng T, Lyngholm LK, Ford CF, Bonson CR (1992) A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130:81–96
Valent B, Farral L, Chumley FG (1991) Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127:87–101
Van Kan JAL, van den Ackerveken GF, De Wit PJGM (1991) Cloning and characterization of cDNA of avirulence gene Avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 4:52–59
van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic maps. Plant Research International, Wageningen
van’t Slot KAE, Knogge W (2002) A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Crit Rev Plant Sci 21:229–271
Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Xu J, Leslie JF (1996) A genetic map of Gibberella fujikuroi matting population A (Fusarium moniliforme). Genetics 143:175–189
Zhong S, Steffenson BJ, Martinez JP, Ciuffetti LM (2002) A molecular genetic map and electrophoretic karyotype of the plant pathogenic fungus Cochliobolus sativus. Mol Plant Microbe Interact 15:481–492
Acknowledgments
We are grateful to Emigdia Alfaro for excellent technical assistance in the AFLP analysis, Octavio Martínez de la Vega for helpful discussions on the statistical and mapping analysis and to Luis Herrera-Estrella for critical reading of the manuscript. This research was supported by grants from CONACyT/SAGAR no. K159-A9702 and SEP-CONACyT grant nos. 28275 and 40369-Q. FLM is also indebted to CONACyT, Mexico for doctoral fellowship no. 120910.
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Luna-Martínez, F., Rodríguez-Guerra, R., Victoria-Campos, M. et al. Development of a molecular genetic linkage map for Colletotrichum lindemuthianum and segregation analysis of two avirulence genes. Curr Genet 51, 109–121 (2007). https://doi.org/10.1007/s00294-006-0111-0
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DOI: https://doi.org/10.1007/s00294-006-0111-0