Abstract
Genetic mapping is a basic tool for eukaryotic genomic research. Linkage maps provide insights into genome organization and can be used for genetic studies of traits of interest. A genetic linkage map is a suitable support for the anchoring of whole genome sequences. It allows the localization of genes of interest or quantitative trait loci (QTL) and map-based cloning. While genetic mapping has been extensively used in plant or animal models, this discipline is more recent in fungi. The present article reviews the current status of genetic linkage map research in fungal species. The process of linkage mapping is detailed, from the development of mapping populations to the construction of the final linkage map, and illustrated based on practical examples. The range of specific applications in fungi is browsed, such as the mapping of virulence genes in pathogenic species or the mapping of agronomically relevant QTL in cultivated edible mushrooms. Future prospects are finally discussed in the context of the most recent advances in molecular techniques and the release of numerous fungal genome sequences.
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Bakkeren G, Jiang G, Warren RL, Butterfield Y, Shin H, Chiu R, Linning R, Schein J, Lee N, Hu G, Kupfer DM, Tang Y, Roe BA, Jones S, Marra M, Kronstad JW (2006) Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet Biol 43(9):655–666
Boone C, Bussey H, Andrews BJ (2007) Exploring genetic interactions and networks with yeast. Nat Rev Genet 8(6):437–449
Borck K, Braymer HD (1974) The genetic analysis of resistance to benomyl in Neurospora crassa. J Gen Microbiol 85(1):51–56
Bowden RL, Leslie JF (1999) Sexual recombination in Gibberella zeae. Phytopathol 89:182–188
Brem RB, Storey JD, Whittle J, Kruglyak L (2005) Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 436(7051):701–703
Broders KD, Woeste KE, San Miguel PJ, Westerman RP, Boland GJ (2011) Discovery of single-nucleotide polymorphisms (SNPs) in the uncharacterized genome of the ascomycete Ophiognomonia clavigignenti-juglandacearum from 454 sequence data. Mol Ecol Resour 11(4):693–702
Broggini GA, Bus VG, Parravicini G, Kumar S, Groenwold R, Gessler C (2011) Genetic mapping of 14 avirulence genes in an EU-B04 x 1639 progeny of Venturia inaequalis. Fungal Genet Biol 48(2):166–176
Celton JM, Christoffels A, Sargent DJ, Xu X, Rees DJ (2010) Genome-wide SNP identification by high-throughput sequencing and selective mapping allows sequence assembly positioning using a framework genetic linkage map. BMC Biol 8:155
Chang SW, Jung G (2008) The first linkage map of the plant-pathogenic basidiomycete Typhula ishikariensis. Genome 51(2):128–136
Cheema J, Dicks J (2009) Computational approaches and software tools for genetic linkage map estimation in plants. Briefings Bioinforma 10(6):595–608
Christians JK, Cheema MS, Vergara IA, Watt CA, Pinto LJ, Chen N, Moore MM (2011) Quantitative trait locus (QTL) mapping reveals a role for unstudied genes in Aspergillus virulence. PLoS One 6(4):e19325
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(5):293–302
Cumagun CJR, Bowden RL, Jurgenson JE, Leslie JF, Miedaner T (2004) Genetic mapping of pathogenicity and aggressiveness of Gibberella zeae (Fusarium graminearum) toward wheat. Phytopathology 94(5):520–526
Cumagan CJR, Parzies HK, Miedaner T (2007) Genetic variation and segregation of DNA polymorphisms in Gibberella zeae detected with AFLP and RAPD markers. Asian J Plant Sci 6(8):1174–1181
Dalman K (2010) Heterobasidion root rot, Genetic mapping of virulence and evolutionay history. Doctoral thesis. Swedish University of Agricultural Sciences, Uppsala
De Vos L, Myburg AA, Wingfield MJ, Desjardins AE, Gordon TR, Wingfield BD (2007) Complete genetic linkage maps from an interspecific cross between Fusarium circinatum and Fusarium subglutinans. Fungal Genet Biol 44(8):701–714
Debets AJM, Swart K, Bos CJ (1990) Genetic analysis of Aspergillus niger: isolation of chlorate resistance mutants, their use in mitotic mapping and evidence for an eighth linkage group. Mol Gen Genet 221(3):453–458
Dutech C, Enjalbert J, Fournier E, Delmotte F, Barres B, Carlier J, Tharreau D, Giraud T (2007) Challenges of microsatellite isolation in fungi. Fungal Genet Biol 44(10):933–949
Ehrenreich IM, Gerke JP, Kruglyak L (2009) Genetic dissection of complex traits in yeast: insights from studies of gene expression and other phenotypes in the BYxRM cross. Cold Spring Harb Symp Quant Biol 74:145–153
Ellwood SR, Liu Z, Syme RA, Lai Z, Hane JK, Keiper F, Moffat CS, Oliver RP, Friesen TL (2010) A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol 11(11):R109
Ferreira A, Da Silva MF, da Costa L, da Costa e Silva, Cruz CD (2006) Estimating the effects of population size and type on the accuracy of genetics maps. Genet Mol Biol 29(1):187–192
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(3):189–203
Forche A, Magee PT, Magee BB, May G (2004) Genome-wide single-nucleotide polymorphism map for Candida albicans. Eukaryot Cell 3(3):705–714
Foulongne-Oriol M, Spataro C, Cathalot V, Monllor S, Savoie JM (2010) An expanded genetic linkage map of an intervarietal Agaricus bisporus var. bisporus x A. bisporus var. burnettii hybrid based on AFLP, SSR and CAPS markers sheds light on the recombination behaviour of the species. Fungal Genet Biol 47(3):226–236
Foulongne-Oriol M, Dufourcq R, Spataro C, Devesse C, Broly A, Rodier A, Savoie JM (2011a) Comparative linkage mapping in the white button mushroom Agaricus bisporus provides foundation for breeding management. Curr Genet 57(1):39–50
Foulongne-Oriol M, Minvielle N, Savoie JM (2011b) QTL for resistance to Trichoderma lytic enzymes and metabolites in Agaricus bisporus. 7th International Conference on Mushroom Biology and Mushroom Products, Arcachon, France
Foulongne-Oriol M, Rodier A, Rousseau T, Savoie JM (2012a) QTL mapping of yield-related components and oligogenic control of the cap colour in the button mushroom Agaricus bisporus. Appl Environ Microbiol. 78(7):2422–2434
Foulongne-Oriol M, Rodier A, Savoie JM (2012b) Relationship between yield components and partial resistance to Lecanicillium fungicola in Agaricus bisporus assessed by QTL mapping. Appl Environ Microbiol. 78(7):2435–2442
Frankel C, Ellingboe AH (1977) New mutations and a 7-chromosome linkage map of Schizophyllum commune. Genetics 85(3):417–425
Frenkel O, Portillo I, Brewer MT, Péros JP, Cadle-Davidson L, Milgroom MG (2012) Development of microsatellite markers from the transcriptome of Erysiphe necator for analysing population structure in North America and Europe. Plant Pathol 61(1):106–119
Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent MH, Rouxel T (2007) Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant Microbe Interact 20(4):459–470
Gale LR, Bryant JD, Calvo S, Giese H, Katan T, O'Donnell K, Suga H, Taga M, Usgaard TR, Ward TJ, Kistler HC (2005) Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics 171(3):985–1001
Gallegos A, Jacobson DJ, Raju NB, Skupski MP, Natvig DO (2000) Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics 154(2):623–633
Goodwin SB, van der Lee TA, Cavaletto JR, Te Lintel Hekkert B, Crane CF, Kema GH (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(5):398–414
Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent MH, Rouxel T (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60(1):67–80
Gupta PK, Rustgi S, Mir RR (2008) Array-based high-throughput DNA markers for crop improvement. Heredity 101(1):5–18
Imbernon M, Callac P, Gasqui P, Kerrigan RW, Velcko AJ (1996) BSN, the primary determinant of basidial spore number and reproductive mode in Agaricus bisporus, maps to chromosome I. Mycologia 88(5):749–761
Jones N, Ougham H, Thomas H, Pasakinskiene I (2009) Markers and mapping revisited: finding your gene. New Phytol 183(4):935–966
Jurgenson JE, Bowden RL, Zeller KA, Leslie JF, Alexander NJ, Plattner RD (2002a) A genetic map of Gibberella zeae (Fusarium graminearum). Genetics 160(4):1451–1460
Jurgenson JE, Zeller KA, Leslie JF (2002b) Expanded genetic map of Gibberella moniliformis (Fusarium verticillioides). Appl Environ Microbiol 68(4):1972–1979
Kaye C, Milazzo J, Rozenfeld S, Lebrun MH, 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(3):207–214
Kema GH, Goodwin SB, Hamza S, Verstappen EC, Cavaletto JR, Van der Lee TA, de Weerdt M, Bonants PJ, Waalwijk C (2002) A combined amplified fragment length polymorphism and randomly amplified polymorphism DNA genetic kinkage map of Mycosphaerella graminicola, the septoria tritici leaf blotch pathogen of wheat. Genetics 161(4):1497–1505
Kerrigan RW (1992) Strategies for the efficient recovery of Agaricus bisporus homokaryons. Mycologia 84(4):575–579
Kerrigan RW, Royer JC, Baller LM, Kohli Y, Horgen PA, Anderson JB (1993) Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics 133(2):225–236
Kim TS, Logsdon BA, Park S, Mezey JG, Lee K (2007) Quantitative trait loci for the circadian clock in Neurospora crassa. Genetics 177(4):2335–2347
Kim TS, Booth JG, Gauch HG Jr, Sun Q, Park J, Lee YH, Lee K (2008) Simple sequence repeats in Neurospora crassa: distribution, polymorphism and evolutionary inference. BMC Genomics 9:31
Krejci R, Homolka L (1991) Genetic-mapping in the lignin-degrading basidiomycete Phanerochaete-chrysosporium. Appl Environ Microbiol 57(1):151–156
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(6):453–463
Kubisiak TL, Anderson CL, Amerson HV, Smith JA, Davis JM, Nelson CD (2011) A genomic map enriched for markers linked to Avr1 in Cronartium quercuum f.sp. fusiforme. Fungal Genet Biol 48(3):266–274
Labbe J, Zhang X, Yin T, Schmutz J, Grimwood J, Martin F, Tuskan GA, Le Tacon F (2008) A genetic linkage map for the ectomycorrhizal fungus Laccaria bicolor and its alignment to the whole-genome sequence assemblies. New Phytol 180(2):316–328
Labbe J, Murat C, Morin E, Le Tacon F, Martin F (2011) Survey and analysis of simple sequence repeats in the Laccaria bicolor genome, with development of microsatellite markers. Curr Genet 57(2):75–88
Lai Z, Faris JD, Weiland JJ, Steffenson BJ, Friesen TL (2007) Genetic mapping of Pyrenophora teres f. teres genes conferring avirulence on barley. Fungal Genet Biol 44:323–329
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1(2):174–181
Larraya LM, Perez G, Ritter E, Pisabarro AG, Ramirez L (2000) Genetic linkage map of the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 66(12):5290–5300
Larraya LM, Perez G, Iribarren I, Blanco JA, Alfonso M, Pisabarro AG, Ramirez L (2001) Relationship between monokaryotic growth rate and mating type in the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 67(8):3385–3390
Larraya LM, Idareta E, Arana D, Ritter E, Pisabarro AG, Ramirez L (2002) Quantitative trait loci controlling vegetative growth rate in the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 68(3):1109–1114
Larraya LM, Alfonso M, Pisabarro AG, Ramirez 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 69(6):3617–3625
Lee J, Jurgenson JE, Leslie JF, Bowden RL (2008) Alignment of genetic and physical maps of Gibberella zeae. Appl Environ Microbiol 74(8):2349–2359
Lind M, Olson A, Stenlid J (2005) An AFLP-markers based genetic linkage map of Heterobasidion annosum locating intersterility genes. Fungal Genet Biol 42(6):519–527
Lind M, Stenlid J, Olson A (2007a) Genetics and QTL mapping of somatic incompatibility and intraspecific interactions in the basidiomycete Heterobasidion annosum s.l. Fungal Genet Biol 44(12):1242–1251
Lind M, Dalman K, Stenlid J, Karlsson B, Olson A (2007b) Identification of quantitative trait loci affecting virulence in the basidiomycete Heterobasidion annosum s.l. Curr Genet 52(1):35–44
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(1):99–111
Loftus M, Bouchti-King L, Robles C (2000) Use of SCAR marker for cap color in Agaricus bisporus breeding programs. Mushroom Sci 15:201–205
Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breed. doi:10.1007/s11032-012-9706-y
Luna-Martinez F, Rodriguez-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 Genet 51(2):109–121
Malausa T, Gilles A, Meglecz E, Blanquart H, Duthoy S, Costedoat C, Dubut V, Pech N, Castagnone-Sereno P, Delye C, Feau N, Frey P, Gauthier P, Guillemaud T, Hazard L, Le Corre V, Lung-Escarmant B, Male PJ, Ferreira S, Martin JF (2011) High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Mol Ecol Resour 11(4):638–644
Malkus A, Song QJ, Cregan P, Arseniuk E, Ueng PP (2009) Genetic linkage map of Phaeosphaeria nodorum, the causal agent of Stagonospora nodorum blotch disease of wheat. Eur J Plant Pathol 124(4):681–690
Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12(12):930–932
Manzo-Sanchez G, Zapater MF, Luna-Martinez F, Conde-Ferraez L, Carlier J, James-Kay A, Simpson J (2008) Construction of a genetic linkage map of the fungal pathogen of banana Mycosphaerella fijiensis, causal agent of black leaf streak disease. Curr Genet 53(5):299–311
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(2):619–631
Martinez-Rossi NM, Azevedo JL (1989) Characterization of benomyl resistance mutants of Aspergillus nidulans. Rev Bras Genet 12(3):477–484
Merino ST, Nelson MA, Jacobson DJ, Natvig DO (1996) Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics 143(2):789–799
Miyazaki K, Huang FX, Zhang BX, Shiraishi S, Sakai M, Shimaya C, Shishido K (2008) Genetic map of a basidiomycete fungus, Lentinula edodes (shiitake mushroom), constructed by tetrad analysis. Breed Sci 58(1):23–30
Moquet F, Desmerger C, Mamoun M, Ramos-Guedes-Lafargue M, Olivier JM (1999) A quantitative trait locus of Agaricus bisporus resistance to Pseudomonas tolaasii is closely linked to natural cap color. Fungal Genet Biol 28(1):34–42
Muraguchi H, Ito Y, Kamada T, Yanagi SO (2003) A linkage map of the basidiomycete Coprinus cinereus based on random amplified polymorphic DNAs and restriction fragment length polymorphisms. Fungal Genet Biol 40(2):93–102
Murat C, Riccioni C, Belfiori B, Cichocki N, Labbe J, Morin E, Tisserant E, Paolocci F, Rubini A, Martin F (2011) Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genet Biol 48(6):592–601
Nitta N, Farman ML, Leong SA (1997) Genome organization of Magnaporthe grisea: integration of genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Applied Genet 95(1–2):20–32
Okuda Y, Murakami S, Matsumoto T (2009) Development of STS markers suitable for marker assisted selection of sporeless trait in oyster mushroom, Pleurotus pulmonarius. Breed Sci 59:315–319
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(3):235–246
Perez G, Pangilinan J, Pisabarro AG, Ramirez L (2009) Telomere organization in the ligninolytic basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 75(5):1427–1436
Perkins DD, Radford A, Newmeyer D, Bjorkman M (1982) Chromosomal loci of Neurospora crassa. Microbiol Rev 46(4):426–570
Peters JL, Cnudde F, Gerats T (2003) Forward genetics and map-based cloning approaches. Trends Plant Sci 8(10):484–491
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(5):373–381
Piepho HP (2000) Optimal marker density for interval mapping in a backcross population. Heredity 84(4):437–440
Ritter E, Salamini F (1996) The calculation of recombination frequencies in crosses of allogamous plant species with applications to linkage mapping. Genet Res 67(1):55–65
Samils N, Olson A, Stenlid J (2008) The capacity in Heterobasidion annosum s.l. to resist overgrowth by the biocontrol agant Phlebiopsis gigantea is a heritable trait. Biol Control 45:419–426
Santoyo F, Gonzalez A, Terron M, Ramirez L, Pisabarro AG (2008) Quantitative linkage mapping of lignin-degrading enzymatic activities in Pleurotus ostreatus. Enzym Microb Technol 43:137–143
Sonnenberg ASM, Baars JJP, Hendrickx PM, Kerrigan RW (2005) Breeding mushroom: state of the art. Acta Edulis Fungi (Suppl) 12:163–173
Stajich JE, Wilke SK, Ahren D, Au CH, Birren BW, Borodovsky M, Burns C, Canback B, Casselton LA, Cheng CK, Deng J, Dietrich FS, Fargo DC, Farman ML, Gathman AC, Goldberg J, Guigo R, Hoegger PJ, Hooker JB, Huggins A, James TY, Kamada T, Kilaru S, Kodira C, Kues U, Kupfer D, Kwan HS, Lomsadze A, Li W, Lilly WW, Ma LJ, Mackey AJ, Manning G, Martin F, Muraguchi H, Natvig DO, Palmerini H, Ramesh MA, Rehmeyer CJ, Roe BA, Shenoy N, Stanke M, Ter-Hovhannisyan V, Tunlid A, Velagapudi R, Vision TJ, Zeng Q, Zolan ME, Pukkila PJ (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci U S A 107(26):11889–11894
Stam P (1993) Construction of integrated genetic-linkage maps by means of a new computer package—Joinmap. Plant J 3(5):739–744
Sturtevant AH (1913) The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J of Exp Zool 14:43–59
Terashima K, Matsumoto T, Hayashi E, Fukumasa-Nakai Y (2002) A genetic linkage map of Lentinula edodes (shiitake) based on AFLP markers. Mycol Res 106:911–917
Terashima K, Matsumoto T, Hayashi E, Kawasaki S, Fukumasa-Nakai Y (2006) Construction of a linkage map of Lentinula edodes (shiitake) with the HEGS (high efficiency genome scanning) system: use of versatil AFLP and PCR-based gene markers. Mycoscience 47:336–346
Teunissen HA, Rep M, Houterman PM, Cornelissen BJ, Haring MA (2003) Construction of a mitotic linkage map of Fusarium oxysporum based on Foxy-AFLPs. Mol Genet Genomics 269(2):215–226
van Berloo R (2008) GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 99(2):232–236
van der Nest MA, Slippers B, Steenkamp ET, De Vos L, Van Zyl K, Stenlid J, Wingfield MJ, Wingfield BD (2009) Genetic linkage map for Amylostereum areolatum reveals an association between vegetative growth and sexual and self recognition. Fungal Genet Biol 46(9):632–641
Vignal A, Milan D, SanCristobal M, Eggen A (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genet Sel Evol 34(3):275–305
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78
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(21):4407–4414
Wang X, Mulock B, Guus B, McCallum B (2010) Development of EST-derived simple sequence repeat markers for wheat leaf rust fungus, Puccinia triticina Eriks. Can J Plant Pathol 32(1):98–107
Wittenberg AH, van der Lee TA, Ben M'barek S, Ware SB, Goodwin SB, Kilian A, Visser RG, Kema GH, Schouten HJ (2009) Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4(6):e5863
Xu JR, Leslie JF (1996) A genetic map of Gibberella fujikuroi mating population A (Fusarium moniliforme). Genetics 143(1):175–189
Xu JP, Kerrigan RW, Horgen PA, Anderson JB (1993) Localization of the Mating type gene in Agaricus bisporus. Appl Environ Microbiol 59(9):3044–3049
Xu J, Guo H, Yang ZL (2007) Single nucleotide polymorphisms in the ectomycorrhizal mushroom Tricholoma matsutake. Microbiology 153(Pt 7):2002–2012
Xu X, Roberts T, Barbara D, Harvey NG, Gao L, Sargent DJ (2009) A genetic linkage map of Venturia inaequalis, the causal agent of apple scab. BMC Res Notes 2:163
Young ND (2000) Constructing a plant genetic linkage map with DNA markers. In: Phillips RL, Vasil JK (eds) DNA-based markers in plants. Kluwer Academic Publishers, Netherlands, pp 31–47
Zambino PJ, Kubelik AR, Szabo LJ (2000) Gene action and linkage of avirulence genes to dna markers in the rust fungus Puccinia graminis. Phytopathology 90(8):819–826
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(5):481–492
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Foulongne-Oriol, M. Genetic linkage mapping in fungi: current state, applications, and future trends. Appl Microbiol Biotechnol 95, 891–904 (2012). https://doi.org/10.1007/s00253-012-4228-4
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DOI: https://doi.org/10.1007/s00253-012-4228-4