Which MAT gene? Pezizomycotina (Ascomycota) mating-type gene nomenclature reconsidered

Ait Benkhali, 2013, A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina, PLoS Genet., 9, e1003642, 10.1371/journal.pgen.1003642 Altschul, 1990, Basic local alignment search tool, J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 Amselem, 2011, Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea, PLoS Genet., 7, e1002230, 10.1371/journal.pgen.1002230 Arie, 1997, Efficient cloning of Ascomycete mating type genes by PCR amplification of the conserved MAT HMG box, Fungal Genet. Biol., 21, 118, 10.1006/fgbi.1997.0961 Arie, 2000, Mating-type genes from asexual phytopathogenic ascomycetes Fusarium oxysporum and Alternaria alternata, Mol. Plant Microbe Interact., 13, 1330, 10.1094/MPMI.2000.13.12.1330 Arnaise, 1993, Heterologous expression of mating-type genes in filamentous fungi, Proc. Natl. Acad. Sci. U.S.A., 90, 6616, 10.1073/pnas.90.14.6616 Arnaise, 2001, Mutations in mating-type genes of the heterothallic fungus Podospora anserina lead to self-fertility, Genetics, 159, 545, 10.1093/genetics/159.2.545 Arzanlou, 2010, Evolutionary dynamics of mating-type loci of Mycosphaerella spp. occurring on banana, Eukaryot. Cell, 9, 164, 10.1128/EC.00194-09 Aylward, 2016, Genetic basis for high population diversity in Protea-associated Knoxdaviesia, Fungal Genet. Biol., 96, 47, 10.1016/j.fgb.2016.10.002 Barratt, 1965, Neurospora genetic nomenclature, Neurospora Newsl., 8, 23 Barve, 2003, Cloning and characterization of the mating type (MAT) locus from Ascochyta rabiei (teleomorph: Didymella rabiei) and a MAT phylogeny of legume-associated Ascochyta spp., Fungal Genet. Biol., 39, 151, 10.1016/S1087-1845(03)00015-X Bennett, 2003, Identity and conservation of mating type genes in geographically diverse isolates of Phaeosphaeria nodorum, Fungal Genet. Biol., 40, 25, 10.1016/S1087-1845(03)00062-8 Benson, 2013, GenBank, Nucleic Acids Res., 41, D36, 10.1093/nar/gks1195 Bihon, 2014, MAT gene idiomorphs suggest a heterothallic sexual cycle in a predominantly asexual and important pine pathogen, Fungal Genet. Biol., 62, 55, 10.1016/j.fgb.2013.10.013 Billiard, 2011, Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types, Biol. Rev. Camb. Philos. Soc., 86, 421, 10.1111/j.1469-185X.2010.00153.x Billiard, 2012, Sex, outcrossing and mating types: unsolved questions in fungi and beyond, J. Evol. Biol., 25, 1020, 10.1111/j.1420-9101.2012.02495.x Bin Terhem, 2015, Mating type and sexual fruiting body of Botrytis elliptica, the causal agent of fire blight in lily, Eur. J. Plant Pathol., 142, 615, 10.1007/s10658-015-0639-2 Birney, 2004, GeneWise and genomewise, Genome Res., 14, 988, 10.1101/gr.1865504 Bistis, 1998, Physiological heterothallism and sexuality in Euascomycetes: a partial history, Fungal Genet. Biol., 23, 213, 10.1006/fgbi.1998.1050 Blakeslee, 1904, Sexual reproduction in the Mucorineae, Proc. Am. Acad. Arts Sci., 40, 205, 10.2307/20021962 Bubnick, 2007, The MAT1 locus of Histoplasma capsulatum is responsive in a mating type-specific manner, Eukaryot. Cell, 6, 616, 10.1128/EC.00020-07 Butler, 2007, The evolution of MAT: the ascomycetes, 3 Cantarel, 2008, MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes, Genome Res., 18, 188, 10.1101/gr.6743907 Chitrampalam, 2013, The Sclerotinia sclerotiorum mating type locus (MAT) contains a 3.6-kb region that is inverted in every meiotic generation, PLoS One, 8, e56895, 10.1371/journal.pone.0056895 Cisar, 1999, Mating system of the filamentous ascomycete, Glomerella cingulata, Curr. Genet., 35, 127, 10.1007/s002940050441 Cisar, 1994, Sequence similarity of mating-type idiomorphs: a method which detects similarity among the Sordariaceae fails to detect similar sequences in other filamentous ascomycetes, Mycologia, 86, 540, 10.2307/3760747 Civetta, 1998, Sex-related genes, directional sexual selection, and speciation, Mol. Biol. Evol., 15, 901, 10.1093/oxfordjournals.molbev.a025994 Coelho, 2008, Identification of mating type genes in the bipolar basidiomycetous yeast Rhodosporidium toruloides: first insight into the MAT locus structure of the Sporidiobolales, Eukaryot. Cell, 7, 1053, 10.1128/EC.00025-08 Cohen, 1973, Construction of biologically functional bacterial plasmids in vitro, Proc. Natl. Acad. Sci. U. S. A., 70, 3240, 10.1073/pnas.70.11.3240 Comeau, 2015, Functional annotation of the Ophiostoma novo-ulmi genome: insights into the phytopathogenicity of the fungal agent of Dutch elm disease, Genome Biol. Evol., 7, 410, 10.1093/gbe/evu281 Conde-Ferráez, 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, 10.1111/j.1364-3703.2006.00376.x Davis, 2004, The age of model organisms, Nat. Rev. Genet., 5, 69, 10.1038/nrg1250 Debuchy, 2010, Mating systems and sexual morphogenesis in Ascomycetes, 501 Debuchy, 1992, The mating types of Podospora anserina: functional analysis and sequence of the fertilization domains, Mol. Gen. Genet., 233, 113, 10.1007/BF00587568 Debuchy, 2006, Mating-type structure, evolution, and function in Euascomycetes, 293, 10.1007/3-540-28135-5_15 DiGuistini, 2011, Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen, Proc. Natl. Acad. Sci. U. S. A., 108, 2504, 10.1073/pnas.1011289108 Dyer, 1994, Seasonal development of apothecia of the cereal eyespot pathogen Tapesia yallundae on straw stubble in the UK, Ann. Appl. Biol., 125, 489, 10.1111/j.1744-7348.1994.tb04986.x Dyer, 2016, Mating-type structure, function, regulation and evolution in the Pezizomycotina, 351 Dyer, 2003, Genomics reveals sexual secrets of Aspergillus, Microbiology, 149, 2301, 10.1099/mic.0.C0119-0 Foster, 2003, Isolation and characterisation of the mating-type (MAT) locus from Rhynchosporium secalis, Curr. Genet., 44, 277, 10.1007/s00294-003-0445-9 Fraser, 2007, Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii, Eukaryot. Cell, 6, 622, 10.1128/EC.00018-07 Galagan, 2005, Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae, Nature, 438, 1105, 10.1038/nature04341 Giraud, 2008, Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism, Eukaryot. Cell, 7, 765, 10.1128/EC.00440-07 Glass, 1990, Neurospora crassa A mating-type region, Proc. Natl. Acad. Sci. U. S. A., 87, 4912, 10.1073/pnas.87.13.4912 Glass, 1988, DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar, Science, 241, 570, 10.1126/science.2840740 Griffiths, 2010 Grigoriev, 2011, Fueling the future with fungal genomics, Mycologia, 2, 192 Groenewald, 2006, Mating type gene analysis in apparently asexual Cercospora species is suggestive of cryptic sex, Fungal Genet. Biol., 43, 813, 10.1016/j.fgb.2006.05.008 Grosschedl, 1994, HMG domain proteins: architectural elements in the assembly of nucleoprotein structures, Trends Genet., 10, 94, 10.1016/0168-9525(94)90232-1 Hibbett, 2007, A higher-level phylogenetic classification of the Fungi, Mycol. Res., 111, 509, 10.1016/j.mycres.2007.03.004 Hyatt, 2000, Improved analysis and annotation tools for whole-genome computational annotation and analysis: GRAIL-EXP genome analysis toolkit and related analysis tools Idnurm, 2011, Sex and speciation: the paradox that non-recombining DNA promotes recombination, Fungal Biol. Rev., 25, 121, 10.1016/j.fbr.2011.07.003 Inderbitzin, 2006, Systematics and mating systems of two fungal pathogens of opium poppy: the heterothallic Crivellia papaveracea with a Brachycladium penicillatum asexual state and a homothallic species with a Brachycladium papaveris asexual state, Can. J. Bot., 84, 1304, 10.1139/b06-067 Jackson, 1972, Biochemical method for inserting new genetic information into DNA of Simian Virus 40: circular SV40 DNA molecules containing lambda phage genes and the galactose operon of Escherichia coli, Proc. Natl. Acad. Sci. U. S. A., 69, 2904, 10.1073/pnas.69.10.2904 Jacobi, 2010, Identification of transcripts up-regulated in asexual and sexual fruiting bodies of the Dutch elm disease pathogen Ophiostoma novo-ulmi, Can. J. Microbiol., 56, 697, 10.1139/W10-053 Kanamori, 2007, Novel mating type-dependent transcripts at the mating type locus in Magnaporthe oryzae, Gene, 403, 6, 10.1016/j.gene.2007.06.015 Kanematsu, 2007, Mating-type loci of heterothallic Diaporthe spp.: homologous genes are present in opposite mating-types, Curr. Genet., 52, 11, 10.1007/s00294-007-0132-3 Kang, 1994, Isolation of the mating-type genes of the phytopathogenic fungus Magnaporthe grisea using genomic subtraction, Genetics, 138, 289, 10.1093/genetics/138.2.289 Karlsson, 2015, Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea, Genome Biol. Evol., 7, 465, 10.1093/gbe/evu292 Klix, 2010, Functional characterization of MAT1-1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and nonessential sexual regulators, Eukaryot. Cell, 9, 894, 10.1128/EC.00019-10 Laudet, 1993, Ancestry and diversity of the HMG box superfamily, Nucleic Acids Res., 21, 2493, 10.1093/nar/21.10.2493 Lee, 2010, The evolution of sex: a perspective from the fungal kingdom, Microbiol. Mol. Biol. Rev., 74, 298, 10.1128/MMBR.00005-10 Li, 2010, Organization and evolutionary trajectory of the mating type (MAT) locus in dermatophyte and dimorphic fungal pathogens, Eukaryot. Cell, 9, 46, 10.1128/EC.00259-09 Li, 2013, Identification of the mating-type (MAT) locus that controls sexual reproduction of Blastomyces dermatitidis, Eukaryot. Cell, 12, 109, 10.1128/EC.00249-12 Lindegren, 1936, A six-point map of the sex-chromosome of Neurospora crassa, J. Genet., 32, 243, 10.1007/BF02982680 Lindegren, 1936, The structure of the sex-chromosomes of Neurospora crassa: suggested by genetical analysis, J. Hered., 27, 251, 10.1093/oxfordjournals.jhered.a104220 Mandel, 2007, Genomic and population analyses of the mating type loci in Coccidioides species reveal evidence for sexual reproduction and gene acquisition, Eukaryot. Cell, 6, 1189, 10.1128/EC.00117-07 Martin, 2011, Structure and evolution of the Fusarium mating type locus: new insights from the Gibberella fujikuroi complex, Fungal Genet. Biol., 48, 731, 10.1016/j.fgb.2011.03.005 Martin, 2010, Tracing the origin of the fungal α1 domain places its ancestor in the HMG-box superfamily: implication for fungal mating-type evolution, PLoS One, 5, 13, 10.1371/journal.pone.0015199 Martinez, 2004, Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78, Nat. Biotechnol., 22, 695, 10.1038/nbt967 McCartney, 1990, The production and release of ascospores of Pyrenopeziza brassicae on oilseed rape, Plant Pathol., 39, 17, 10.1111/j.1365-3059.1990.tb02471.x McGuire, 2001, Analysis of mating-type genes in the chestnut blight fungus, Cryphonectria parasitica, Fungal Genet. Biol., 34, 131, 10.1006/fgbi.2001.1295 Metzenberg, 1990, Mating type and mating strategies in Neurospora, Bioessays, 12, 53, 10.1002/bies.950120202 Muller, 2010, Model organisms – a historical perspective, J. Proteom., 73, 2054, 10.1016/j.jprot.2010.08.002 Nødvig, 2015, A CRISPR-Cas9 system for genetic engineering of filamentous fungi, PLoS One, 10, e0133085, 10.1371/journal.pone.0133085 Palmer, 2014, Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white-nose syndrome of bats, G3, 4, 1755, 10.1534/g3.114.012641 Paoletti, 2005, Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus, Curr. Biol., 15, 1242, 10.1016/j.cub.2005.05.045 Paoletti, 2007, Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans, Curr. Biol., 17, 1384, 10.1016/j.cub.2007.07.012 Perkins, 1982, Chromosomal loci of Neurospora crassa, Microbiol. Rev., 46, 426, 10.1128/MMBR.46.4.426-570.1982 Picard, 1991, Cloning the mating types of the heterothallic fungus Podospora anserina: developmental features of haploid transformants carrying both mating types, Genetics, 128, 539, 10.1093/genetics/128.3.539 Pöggeler, 2001, Mating-type genes for classical strain improvements of ascomycetes, Appl. Microbiol. Biotechnol., 56, 589, 10.1007/s002530100721 Pöggeler, 2002, Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus, Curr. Genet., 42, 153, 10.1007/s00294-002-0338-3 Pöggeler, 2000, Comparative analysis of the mating-type loci from Neurospora crassa and Sordaria macrospora: identification of novel transcribed ORFs, Mol. Gen. Genet., 263, 292, 10.1007/s004380051171 Reddy, 2015, The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification, Nucleic Acids Res., 43, D1099, 10.1093/nar/gku950 Rydholm, 2007, DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri, Eukaryot. Cell, 6, 868, 10.1128/EC.00319-06 Saiki, 1988, Primer-directed enzymatic amplification of DNA, Science, 239, 487, 10.1126/science.2448875 Sanger, 1975, A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase, J. Mol. Biol., 94, 441, 10.1016/0022-2836(75)90213-2 Sanger, 1977, DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. U. S. A., 74, 5463, 10.1073/pnas.74.12.5463 Singh, 1998, Cloning of the mating type loci from Pyrenopeziza brassicae reveals the presence of a novel mating type gene within a discomycete MAT 1-2 locus encoding a putative metallothionein-like protein, Mol. Microbiol., 30, 799, 10.1046/j.1365-2958.1998.01112.x Singh, 1999, Intra-specific and inter-specific conservation of mating-type genes from the discomycete plant-pathogenic fungi Pyrenopeziza brassicae and Tapesia yallundae, Curr. Genet., 36, 290, 10.1007/s002940050503 Solovyev, 2006, Automatic annotation of eukaryotic genes, pseudogenes and promoters, Genome Biol., 7, S10.11 Soullier, 1999, Diversification pattern of the HMG and SOX family members during evolution, J. Mol. Evol., 48, 517, 10.1007/PL00006495 Staben, 1990, Neurospora crassa a mating-type region, Proc. Natl. Acad. Sci. U. S. A., 87, 4917, 10.1073/pnas.87.13.4917 Stanke, 2006, AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome, Genome Biol., 7, S11.11 Teixeira, 2015, Asexual propagation of a virulent clone complex in a human and feline outbreak of sporotrichosis, Eukaryot. Cell, 14, 158, 10.1128/EC.00153-14 Thirumoorthy, 2007, Metallothionein: an overview, World J. Gastroenterol., 13, 993, 10.3748/wjg.v13.i7.993 Tsui, 2013, Unequal recombination and evolution of the mating-type (MAT) loci in the pathogenic fungus Grosmannia clavigera and relatives, G3, 3, 465, 10.1534/g3.112.004986 Turgeon, 1998, Application of mating type gene technology to problems in fungal biology, Annu. Rev. Phytopathol., 36, 115, 10.1146/annurev.phyto.36.1.115 Turgeon, 2007, Cochliobolus and Podospora: mechanisms of sex determination and the evolution of reproductive lifestyle, 93 Turgeon, 2000, Proposed nomenclature for mating type genes of filamentous ascomycetes, Fungal Genet. Biol., 31, 1, 10.1006/fgbi.2000.1227 Vaghefi, 2014, Identification of the MAT1 locus in Stagonosporopsis tanaceti, and exploring its potential for sexual reproduction in Australian pyrethrum fields, Fungal Biol., 119, 408, 10.1016/j.funbio.2014.04.004 Van der Nest, 2014, Draft genomes of Amanita jacksonii, Ceratocystis albifundus, Fusarium circinatum, Huntiella omanensis, Leptographium procerum, Rutstroemia sydowiana, and Sclerotinia echinophila, IMA Fungus, 5, 472, 10.5598/imafungus.2014.05.02.11 Waalwijk, 2002, Isolation and characterization of the mating-type idiomorphs from the wheat septoria leaf blotch fungus Mycosphaerella graminicola, Fungal Genet. Biol., 35, 277, 10.1006/fgbi.2001.1322 Wang, 2016, Mating type and simple sequence repeat markers indicate a clonal population of Phyllosticta citricarpa in Florida, Phytopathology, 106, 1300, 10.1094/PHYTO-12-15-0316-R Whitehouse, 1949, Heterothallism and sex in the fungi, Biol. Rev. Camb. Philos. Soc., 24, 411, 10.1111/j.1469-185X.1949.tb00582.x Wilken, 2014, DNA loss at the Ceratocystis fimbriata mating locus results in self-sterility, PLoS One, 9, e92180, 10.1371/journal.pone.0092180 Wilson, 2015, Unisexual reproduction in Huntiella moniliformis, Fungal Genet. Biol., 80, 1, 10.1016/j.fgb.2015.04.008 Wilson, 2015, Homothallism: an umbrella term for describing diverse sexual behaviours, IMA Fungus, 6, 207, 10.5598/imafungus.2015.06.01.13 Witthuhn, 2000, Deletion of the MAT-2 mating-type gene during uni-directional mating-type switching in Ceratocystis, Curr. Genet., 38, 48, 10.1007/s002940000131 Woo, 2006, Genomic and experimental evidence for a potential sexual cycle in the pathogenic thermal dimorphic fungus Penicillium marneffei, FEBS Lett., 580, 3409, 10.1016/j.febslet.2006.05.014 Xu, 2016, Direct repeat-mediated DNA deletion of the mating type MAT1-2 genes results in unidirectional mating type switching in Sclerotinia trifoliorum, Sci. Rep., 6, 27083, 10.1038/srep27083 Yandell, 2012, A beginner's guide to eukaryotic genome annotation, Nat. Rev. Genet., 13, 329, 10.1038/nrg3174 Yoder, 1986, Genetic nomenclature and practice for plant pathogenic fungi, Phytopathology, 76, 383, 10.1094/Phyto-76-383 Yu, 2015, Characterization of mating-type loci in rice false smut fungus Villosiclava virens, FEMS Microbiol. Lett., 362, fnv014, 10.1093/femsle/fnv014 Yun, 2000, Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species, Fungal Genet. Biol., 31, 7, 10.1006/fgbi.2000.1226 Yun, 1999, Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors, Proc. Natl. Acad. Sci. U. S. A., 96, 5592, 10.1073/pnas.96.10.5592 Zaffarano, 2010, Characterization of the mating type (MAT) locus in the Phialocephala fortinii s.l. – Acephala applanata species complex, Fungal Genet. Biol., 47, 761, 10.1016/j.fgb.2010.06.001 Zheng, 2013, The MAT locus genes play different roles in sexual reproduction and pathogenesis in Fusarium graminearum, PLoS One, 8, e66980, 10.1371/journal.pone.0066980