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Current Genetics

, Volume 53, Issue 5, pp 299–311 | Cite as

Construction of a genetic linkage map of the fungal pathogen of banana Mycosphaerella fijiensis, causal agent of black leaf streak disease

  • Gilberto Manzo-Sánchez
  • Marie-Françoise Zapater
  • Francisco Luna-Martínez
  • Laura Conde-Ferráez
  • Jean Carlier
  • Andrew James-KayEmail author
  • June Simpson
Research Article

Abstract

A genetic linkage map of the fungal plant pathogen Mycosphaerella fijiensis, causal agent of black leaf streak disease of banana was developed. A cross between the isolates CIRAD86 (from Cameroon) and CIRAD139A (from Colombia) was analyzed using molecular markers and the MAT locus. The genetic linkage map consists of 298 AFLP and 16 SSR markers with 23 linkage groups, containing five or more markers, covering 1,879 cM. Markers are separated on average by around 5.9 cM. The MAT locus was shown to segregate in a 1:1 ratio but could not be successfully mapped. An estimate of the relation between physical size and genetic distance was approximately 39.0 kb/cM. The estimated total haploid genome size was calculated using the genetic mapping data at 4,298.2 cM. This is the first genetic linkage map reported for this important foliar pathogen of banana. The great utility of the map will be for anchoring contigs in the genome sequence, evolutionary studies in comparison with other fungi, to identify quantitative trait loci (QTLs) associated with aggressiveness or oxidative stress resistance and with the recently available genome sequence, for positional cloning.

Keywords

Ascomycete Mycosphaerella fijiensis Black leaf streak disease of banana Genetic mapping AFLP markers SSR markers 

Notes

Acknowledgments

G. Manzo-Sánchez acknowledges fellowship support from the Consejo Nacional de Ciencia y Tecnología, Mexico (CONACyT) (No. 128982). This project was financially supported by CONACYT (Project No. 37602-B) and the International Network for the Improvement of Banana and Plantain (INIBAP). We thank Emigdia Alfaro for technical support during the AFLP marker analyses.

References

  1. Beadle J, Wright M, McNeely L, Bennet JW (2003) Electrophoretic karyotype analysis in fungi. Adv Appl Microbiol 53:243–270PubMedGoogle Scholar
  2. Bert PF, Gharmet G, Sourdille P, Hayward MD, Balfourer F (1999) A high-density molecular map for the rye grass (Lolium perenne) using AFLP markers. Theor Appl Genet 99:445–452CrossRefGoogle Scholar
  3. Carlier J, Lebrun MH, Zapater M, Dubois C, Mourichon X (1996) Genetic structure of the global population of banana black leaf streak fungus, Mycosphaerella fijiensis. Mol Ecol 5:499–510CrossRefGoogle Scholar
  4. Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:380–390Google Scholar
  5. Conde-Ferráez L, Waalwijk C, Canto-Canché B, Kema GHJ, Crous P, James A, Abeln E (2007) Isolation and characterization of the mating type locus of Mycosphaerella fijiensis, the causal agent of black leaf streak disease of banana. Mol Plant Pathol 8:111–120CrossRefPubMedGoogle Scholar
  6. Cozijnsen AJ, Popa KM, Rolls BD, Purwantara A, Howlett BJ (2000) Genome analysis of the plant pathogenic fungus Leptosphaeria maculans: mapping mating type and host specificity loci. Mol Plant Pathol 1:293–302CrossRefPubMedGoogle Scholar
  7. Cumagun CJR, Borden R, Jurgenson J, Leslie J, Miedaner T (2004) Genetic mapping of pathogenicity and aggressiveness of Gibberella zeae (Fusarium graminearum) toward wheat. Phytopathology 94:520–526CrossRefPubMedGoogle Scholar
  8. 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 31:189–203PubMedCrossRefGoogle Scholar
  9. Fullerton RA, Olsen TL (1995) Pathogenic variability in Mycosphaerella fijiensis Morelet, cause of black sigatoka in banana and plantain. N Z J Crop Hortic Sci 23:39–48Google Scholar
  10. Goodwin SB, van der Lee TAJ, Cavaletto JR, Hekkert BL, Crane CF, Kema GHJ (2007) Identification and genetic mapping of highly polymorphic microsatellite loci from an EST database of the septoria tritici blotch pathogen Mycosphaerella graminicola. Fungal Genet Biol 44:398–414PubMedCrossRefGoogle Scholar
  11. 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 120:947–958PubMedGoogle Scholar
  12. Jurgenson JE, Bowden RL, Zeller KA, Leslie JF, Alexandra NJ, Plattner RD (2002) A genetic map of Gibberella zea (Fusarium graminearum). Genetics 160:1451–1460PubMedGoogle Scholar
  13. Kaye C, Milazzo J, Rozenfeld S, Lebrun M-H, Tharreau D (2003) The development of simple sequence repeat markers for Magnaporthe grisea and their integration into an established genetic linkage map. Fungal Genet Biol 40:207–214PubMedCrossRefGoogle Scholar
  14. Kema GHJ, Goodwin SB, Hamza S, Verstappen 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 161:1497–1505PubMedGoogle Scholar
  15. Kerrigan RW, Royer JC, Baller LM, Kohli Y, Horgen PA, Anderson JB (1992) Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics 133:225–236Google Scholar
  16. 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 43:519–527CrossRefGoogle Scholar
  17. Kupfer DM, Reece CA, Clifton SW, Roe BA, Prade RA (1997) Multicellular ascomycetous fungal genomes contain more than 8,000 genes. Fungal Genet Biol 21:364–372PubMedCrossRefGoogle Scholar
  18. Kwan HS, Xu HL (2002) Construction of a genetic linkage map of shiitake mushroom Lentinula edodes strain L-54. J Biochem Mol Biol 35:465–471PubMedGoogle Scholar
  19. Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 24:842–845Google Scholar
  20. Larraya LM, Perez G, Ritter E, Pisabarro AG, Ramirez L (2000) Genetic linkage map of the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 66:5290–5300PubMedCrossRefGoogle Scholar
  21. Larraya LM, Alfonso M, Pisabarro AG, Ramırez L (2003) Mapping of genomic regions (Quantitative Trait Loci) controlling production and quality in industrial cultures of the edible Basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 68:3617–3625CrossRefGoogle Scholar
  22. Lind M, Olson A, Stenlid J (2005) An AFLP-marker based genetic linkage map of Heterobasidion annosum locating intersterility genes. Fungal Genet Biol 42:519–527PubMedCrossRefGoogle Scholar
  23. Luna-Martinez F (2007) Segregacion de genes de avirulencia y de apareamiento sexual y construccion del mapa de ligamiento de Colletotrichum lindemuthianum, agente causal de la anthracnosis de frijol. Dissertation, 2007, CINVESTAV, Unidad Irapuato, Guanajuato, MexicoGoogle Scholar
  24. Luna-Martínez F, Rodríguez-Guerra R, Victoria-Campos M, Simpson J (2007) Development of a molecular genetic linkage map for Colletotrichum lindemuthianum and segregation analysis of two avirulence genes. Curr Genetics 51:109–121CrossRefGoogle Scholar
  25. Luo C-X, Yin LF, Koyanagi S, Farman ML, Kusaba M, Yaegashi H (2005) Genetic mapping and chrosmosomal assignment of Magnaporthe oryzae avirulence genes AvrPik, AvrPiz, and AvrPiz-t controlling cultivar specificity on rice. Phytopathology 95:640–647CrossRefPubMedGoogle Scholar
  26. Ma J-H, Wang L, Fena S-J, Lin F, Xiao Y, Pan Q-H (2006) Identification and fine mapping of AvrPi15, a novel avirulence gene of Magnaporthe grisea. Theor Appl Genet 113:875–883PubMedCrossRefGoogle Scholar
  27. Marín DH, Romero RA, Guzmán M, Sutton TB (2003) Black sigatoka: an increasing threat to banana cultivation. Plant Dis 87:208–222CrossRefGoogle Scholar
  28. Marra RE, Huang JC, Fung E, Nielsen K, Heitman J, Vilgalys R, Mitchell TG (2004) A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167:619–631PubMedCrossRefGoogle Scholar
  29. May KJ, Whisson SC, Zwart RS, Searle IR, Irwin JAG, Maclean DJ, Carroll BJ, Drenth A (2002) Inheritance and mapping of 11 avirulence genes in Phytophthora sojae. Fungal Genet Biol 37:1–12PubMedCrossRefGoogle Scholar
  30. Mourichon X, Zapater MF (1990) Obtention in vitro du stade Mycosphaerella fijiensis forme parfaite de Cercospora fijiensis. Fruits 45:553–557Google Scholar
  31. Muraguchi H, Ito Y, Kamada T, Yanagi SO (2003) A linkage map of the basidiomycete Coprinus cinereus based on random amplified polymorphic DNA and restriction fragment length polymorphisms. Fungal Genet Biol 40:93–102PubMedCrossRefGoogle Scholar
  32. Neu C, Kaemmer D, Kahl G, Fisches D, Weising K (1999) Polymorphic microsatellite markers for the banana pathogen Mycosphaerella fijiensis. Mol Ecol 8:513–525CrossRefGoogle Scholar
  33. Nitta N, Farman ML, Leong SA (1997) Genome organization of Magnaporthe grisea: integration of genetics maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Appl Genet 95:20–32CrossRefGoogle Scholar
  34. Olson A (2006) Genetic linkage between growth rate and the intersterility genes S and P in the basidiomycete Heterobasidion annosum s. lat. Mycol Res 110:979–984PubMedCrossRefGoogle Scholar
  35. Park SK, Peñas MM, Ramírez L, Pisabarro AG (2006) Genetic linkage map and expression analysis of genes expressed in the lamellae of the edible basidiomycete Pleurotus ostreatus. Fungal Genet Biol 43:376–87PubMedCrossRefGoogle Scholar
  36. 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 35:235–246PubMedCrossRefGoogle Scholar
  37. Phan HTT, Ford R, Taylor PWJ (2003) Mapping the mating type locus of Ascochyta rabiei, the causal agent of ascochyta of chickpea. Mol Plant Pathol 4:373–781CrossRefPubMedGoogle Scholar
  38. Powell L, Thomas WTB, Baird E, Lawrence P, Booth A, Harrower B, McNicol JW, Waugh R (1997) Analysis of quantitative traits in barley by the use of Amplified Fragment Length Polymorphisms. Heredity 79:48–59CrossRefGoogle Scholar
  39. Qi X, Stam P, Lindhout P (1998) Use of locus-specific AFLP markers to construct a high density molecular map in barley. Theor Appl Genet 96:376–384CrossRefGoogle Scholar
  40. Remington DL, Whetten RW, Liu B-H, O´Malley DM (1999) Construction of an AFLP genetic linkage map with near complete genome coverage in Pinus taeda. Theor Appl Genet 98:1279–1292PubMedCrossRefGoogle Scholar
  41. Rivas G-G, Zapater M-F, Abadie C, Carlier J (2004) Founder effects and stochastic dispersal at the continental scale of the fungal pathogen of bananas Mycosphaerella fijiensis. Mol Ecol 13:471–482PubMedCrossRefGoogle Scholar
  42. Rodríguez-García CM, Raigosa-Flores N, Conde-Ferráez L, Peraza-Echeverría L, Canto-Canché B, James-Kay A (2006) Variation in electrophoretic karyotype among Mexican isolates of Mycosphaerella fijiensis. Can J Plant Pathol 28:236–241CrossRefGoogle Scholar
  43. Sicard D, Legg E, Brown S, Babu NK, Ochoa O, Sudarshana P, Michelmore RW (2003) A genetic map of the lettuce downy mildew pathogen, Bremia lactucae, constructed from molecular markers and avirulence genes. Fungal Genet Biol 39:16–30PubMedCrossRefGoogle Scholar
  44. Swart K (1996) Mapping and breeding strategies. In: Bos CJ (ed) Fungal genetics principles and practice. Marcel Dekker, New York, pp 295–315Google Scholar
  45. Teunissen HAS, Rep M, Houterman PM, Cornelissen BJC, Haring MA (2003) Construction of a mitotic linkage map of Fusarium oxysporum based on Foxy-AFLP. Mol Genet Genomics 269:215–226PubMedGoogle Scholar
  46. Van der Lee T, De Witte I, Drenth A, Alfonso C, Govers F (1997) AFLP linkage map of the Oomycete Phytophthora infestans. Fungal Genet Biol 21:278–291PubMedCrossRefGoogle Scholar
  47. Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  48. Vos P, Hogers R, Bleeker M, Reijans M, Van der Lee T, Hornes M, Frijtens A, Pot J, Peleman J, Kiper M, Zabeau M (1995) AFLP, a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  49. Wittenberg AHJ (2006) Genetic mapping using the diversity arrays technology (DArT) :application and validation using the whole-genome sequences of Arabidopsis thaliana and the fungal wheat pathogen Mycosphaerella graminicola. Dissertation, no. 4153, Wageningen UniversityGoogle Scholar
  50. Xu JR, Leslie JE (1996) A genetic map of Gibberella fujikuroi mating population A (Fusarium moniliforme). Genetics 143(1):175–189PubMedGoogle Scholar
  51. Zapater MF, Duchemin M, Dussart JF, Coste D, Brottier P, Carlier J (2008) Microsatellite markers for the fungal banana pathogens Mycosphaerella fijiensis, Mycosphaerella musicola and Mycosphaerella eumusae. Mol Ecol Notes (in press)Google Scholar
  52. Zhong S, Steffenson BJ, Martinez P, Ciuffetti LM (2002) A molecular genetic map and electrophoretic karyotype of the plant pathogenic fungus Cochliobolus sativus. Mol Plant Microbe Interact 15:481–992PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Gilberto Manzo-Sánchez
    • 1
    • 4
  • Marie-Françoise Zapater
    • 2
  • Francisco Luna-Martínez
    • 3
  • Laura Conde-Ferráez
    • 1
  • Jean Carlier
    • 2
  • Andrew James-Kay
    • 1
    Email author
  • June Simpson
    • 3
  1. 1.Unidad de BiotecnologíaCentro de Investigación Científica de YucatánMéridaMexico
  2. 2.UMR BGPI, CIRADMontpellier CEDEX 05France
  3. 3.Departamento de Ingeniería Genética de PlantasCentro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad IrapuatoIrapuatoMexico
  4. 4.Laboratorio de BiotecnologíaFacultad de Ciencias Biológicas y Agropecuarias, Universidad de ColimaTecománMexico

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