Induction of the Sexual Cycle in Filamentous Ascomycetes

  • Chapter
  • First Online:
Genetic Transformation Systems in Fungi, Volume 2

Part of the book series: Fungal Biology ((FUNGBIO))

Abstract

Sexual reproduction provides a valuable tool for strain development and gene identification in fungi, but has been limited in its use because many economically important fungi are only known to reproduce asexually. However, in the past decade a number of publications have reported sexual cycles in supposedly ‘asexual’ fungi, indicating that many presumed asexual fungi might have the potential for sexual reproduction. Methods are therefore described to induce a sexual cycle in various filamentous fungi, including the use of mating-type gene diagnostics to identify compatible mating types in heterothallic ascomycete species, the use of different crossing conditions, and importance of inoculation technique. The conditions for successful mating are often species-specific and it is therefore difficult to give a general protocol. Different methods for the isolation and analysis of ascospore offspring are then described. Finally, ways in which the sexual cycle can be exploited for purposes including gene identification and localization, strain improvement, and gene complementation are covered. It is anticipated that the application of such methodologies will generate sexual progeny with new characteristics or previously unobserved properties.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Notes

  1. 1.

    Commercially made oatmeal agar (OA) is available from certain manufacturers, but in our experience this is not able to induce sex in demanding species. Instead, it is best to prepare OA in house. Different brands of oats can be used and these have can have an effect on the mating. Commonly used brands are Pinhead oatmeal (Odlums, Ireland) and Quaker Oats. For Sordaria and Chaetomium species and Penicillium rubens (P. chrysogenum) this medium needs to be supplemented with biotin (6.4 μg/L) to induce sex (Böhm et al. 2013).

  2. 2.

    In our experience Bacto™ agar is less prone to condensation problems than some cheaper, less pure, commercial agars.

References

  • Aanen DK, Hoekstra RF (2007) Why sex is good: on fungi and beyond. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi: molecular determination and evolutionary principles. ASM, Washington, pp 527–534

    Google Scholar 

  • Arabatzis M, Velegraki A (2013) Sexual reproduction in the opportunistic human pathogen Aspergillus terreus. Mycologia 105:71–79

    PubMed  Google Scholar 

  • Arie T, Christiansen SK, Yoder OC, Turgeon BG (1997) Efficient cloning of ascomycete mating type genes by PCR amplification of the conserved MAT HMG box. Fungal Genet Biol 32:118–130

    Google Scholar 

  • Astell CR, Ahlstrom-Jonasson L, Smith M, Tatchell K, Nasmyth KA, Hall BD (1981) The sequence of the DNAs coding for the mating-type loci of Saccharomyces cerevisiae. Cell 27:15–23

    CAS  PubMed  Google Scholar 

  • Barrs VR, van Doorn TM, Houbraken J, Kidd SE, Martin P, Pinheiro DM, Richardson M, Varga J, Samson RA (2013) Aspergillus felis sp. nov., an emerging agent of invasive aspergillosis in humans, cats and dogs. PLoS One 8:e64871

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bistis GN (1998) Physiological heterothallism and sexuality in euascomycetes: a partial history. Fungal Genet Biol 23:213–222

    PubMed  Google Scholar 

  • Blakeslee AF (1904) Sexual reproduction in the Mucorineae. Proc Natl Acad Sci U S A 40:205–319

    Google Scholar 

  • Böhm J, Hoff B, O’Gorman CM, Wolfers S, Klix V, Binger D, Zadra I, Kürnsteiner H, Pöggeler S, Dyer PS, Kück U (2013) Sexual reproduction and mating-type-mediated strain development in the penicillin-producing fungus Penicillium chrysogenum. Proc Natl Acad Sci U S A 110:1476–1481

    PubMed Central  PubMed  Google Scholar 

  • Burnett J (2003) Fungal populations and species. Oxford University Press, New York

    Google Scholar 

  • Caten CE (1979) Quantitative genetic variation in fungi. In: Thompson JN, Thoday JM (eds) Quantitative genetic variation. Academic, New York, pp 35–59

    Google Scholar 

  • Cavindera B, Trail F (2012) Role of Fig1, a component of the low-affinity calcium uptake system, in growth and sexual development of filamentous fungi. Eukaryot Cell 11:978–988

    Google Scholar 

  • Choi H-W, Kim J-M, Hong S-K, Kim WG, Chun S-C, S-H Y (2009) Mating types and optimum culture conditions for sexual state formation of Fusarium fujikuroi isolates. Mycobiology 37:247–250

    PubMed Central  CAS  PubMed  Google Scholar 

  • Christians JK, Cheema MS, Vergara IA, Watt CA, Pinto LJ, Chen N, Moore MM (2011) Quantitative trait locus (QTL) map** reveals a role for unstudied genes in Aspergillus virulence. PLoS One 6:e19325

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chun SJ, Lee Y-H (1999) Genetic analysis of a mutation on appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett 173:133–137

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Covert SF, Briley A, Wallace MM, McKinney VT (1999) Partial MAT-2 gene structure and the influence of temperature on mating success in Gibberella circinata. Fungal Genet Biol 28:43–54

    CAS  PubMed  Google Scholar 

  • Crous PW, Verkleij GJM, Groenewald JZ, Samson RA (eds) (2009) Fungal biodiversity. CBS laboratory manual series 1. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands

    Google Scholar 

  • Darbyshir HL, van de Vondervoort PJI, Dyer PS (2013) Discovery of sexual reproduction in the black aspergill. Fungal Genet REp 60(Suppl):687

    Google Scholar 

  • Debuchy R, Berteaux-Lecellier V, Silar P (2010) Mating systems and sexual morphogenesis in ascomycetes. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM, Washington, pp 501–535

    Google Scholar 

  • Debuchy R, Turgeon BG (2006) Mating-type structure, evolution, and function in euascomycetes. In: Kües U, Fischer R (eds) The mycota I: growth, differentiation and sexuality. Springer, Berlin, Germany, pp 293–323

    Google Scholar 

  • Dettman JR, Anderson JB, Kohn LM (2010) Genome-wide investigation of reproductive isolation in experimental lineages and natural species of Neurospora: identifying candidate regions by microarray-based genoty** and map**. Evolution 64:694–709

    CAS  PubMed  Google Scholar 

  • Dodge BO (1957) Rib formation in ascospores of Neurospora and questions of terminology. Bull Torrey Bot Club 84:182–188

    Google Scholar 

  • Dyer PS (2007) Sexual reproduction and significance of MAT in the aspergilli. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi: molecular determination and evolutionary principles. ASM, Washington, pp 123–142

    Google Scholar 

  • Dyer PS, Bateman GL, Wood HW (2001a) Development of apothecia of the eyespot pathogen Tapesia on cereal crop stubble residue in England. Plant Pathol 50:356–362

    Google Scholar 

  • Dyer PS, Furneaux PA, Douhan G, Murray TD (2001b) A multiplex PCR test for determination of mating type applied to the plant pathogens Tapesia yallundae and Tapesia acuformis. Fungal Genet Biol 33:173–180

    CAS  PubMed  Google Scholar 

  • Dyer PS, Hansen J, Delaney A, Lucas JA (2000) Genetic control of resistance to the DMI fungicide prochloraz in the cereal eyespot pathogen Tapesia yallundae. Appl Environ Microbiol 66:4599–4604

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dyer PS, Ingram DS, Johnstone K (1992) The control of sexual morphogenesis in the Ascomycotina. Biol Rev 67:421–458

    Google Scholar 

  • Dyer PS, Nicholson P, Lucas JA, Peberdy JF (1995) Genetic control of sexual compatibility in Tapesia yallundae, 79. Abstracts, eighteenth fungal genetics conference, Asilomar. University of California, USA

    Google Scholar 

  • Dyer PS, Nicholson P, Lucas JA, Peberdy JF (1996) Tapesia acuformis as a causal agent of eyespot disease of cereals and evidence for a heterothallic mating system using molecular markers. Mycol Res 100:1219–1226

    CAS  Google Scholar 

  • Dyer PS, Nicholson P, Rezanoor HN, Lucas JA, Peberdy JF (1993) Two-allele heterothallism in Tapesia yallundae, the teleomorph of the cereal eyespot pathogen Pseudocercosporella herpotrichoides. Physiol Mol Plant Pathol 43:403–414

    Google Scholar 

  • Dyer PS, O’Gorman CM (2011) A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol 14:649–654

    PubMed  Google Scholar 

  • Dyer PS, O’Gorman CM (2012) Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol Rev 36:165–192

    CAS  PubMed  Google Scholar 

  • Dyer PS, Paoletti M (2005) Reproduction in Aspergillus fumigatus: sexuality in a supposedly asexual species? Med Mycol 43(Suppl 1):S7–S14

    CAS  PubMed  Google Scholar 

  • Eagle CE (2009) Mating-type genes and sexual potential in the Ascomycete genera Aspergillus and Penicillium. PhD thesis, University of Nottingham, UK

    Google Scholar 

  • Ehrenberg CG (1820) Syzygites, eine neue Schimmelgattung, nebst Beobachtungen über sichtbare Bewegung in Schimmeln. Verhandl. Gesamte Naturf., Freunde, Berlin, pp 98–109

    Google Scholar 

  • Faretra F, Antonacci E, Pollastro S (1988) Sexual behaviour and mating system of Botryotinia fuckeliana, teleomorph of Botrytis cinerea. J Gen Microbiol 134:2543–2550

    Google Scholar 

  • Foulongne-Oriol M (2012) Genetic linkage map** in fungi: current state, applications, and future trends. Appl Microbiol Biotechnol 95:891–904

    CAS  PubMed  Google Scholar 

  • Fraser JA, Stajich JE, Tarcha EJ, Cole GT, Inglis DO, Sil A, Heitman J (2007) Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. Eukaryot Cell 6:622–629

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fresenius G (1863) Beiträge zur Mykologie. H.L. Brönner, Frankfurt, Germany

    Google Scholar 

  • Frisvad JC, Petersen LM, Lyhne K, Larsen TO (2014) Formation of sclerotia and production of indoloterpenes by Aspergillus niger and other species in section Nigri. PLoS One 9:e94857

    PubMed Central  PubMed  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman J, Batzoglou S, Lee SL, Batürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren B (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115

    CAS  PubMed  Google Scholar 

  • Gordon WL (1961) Sex and mating type in relation to the production of perithecia by certain species of Fusarium. Proc Can Phytopathol Soc 28:11

    Google Scholar 

  • Hall C (2013) Quantitative genetics in Neurospora. In: Kasbekar DP, McClusky K (eds) Neurospora genomics and molecular biology. Caister Academic, Norfolk, UK, pp 65–84

    Google Scholar 

  • Han KH, Lee DB, Kim JH, Kim MS, Han KY, Kim WS, Park YS, Kim HB, Han DM (2003) Environmental factors affecting development of Aspergillus nidulans. J Microbiol 41:34–40

    CAS  Google Scholar 

  • Heitman J, Carter DA, Dyer PS, Soll DR (2014) Sexual reproduction of human fungal pathogens. In: Casadevall A, Mitchell AP, Berman J, Kwon-Chung KJ, Perfect JR, Heitman J (eds) Fungal pathogens. Cold Spring Harbour Laboratory Press, New York

    Google Scholar 

  • Henk DA, Eagle CE, Brown K, van den Berg MA, Dyer PS, Peterson SW, Fisher MC (2011) Speciation despite globally overlap** distributions in Penicillium chrysogenum: the population genetics of Alexander Fleming’s lucky fungus. Mol Ecol 20:4288–4301

    CAS  PubMed  Google Scholar 

  • Hoff B, Pöggeler S, Kück U (2008) Eighty years after its discovery, Fleming’s Penicillium strain discloses the secret of its sex. Eukaryot Cell 7:465–470

    PubMed Central  CAS  PubMed  Google Scholar 

  • Horn BW, Moore GG, Carbone I (2009a) Sexual reproduction in Aspergillus flavus. Mycologia 101:423–429

    PubMed  Google Scholar 

  • Horn BW, Moore GG, Carbone I (2011) Sexual reproduction in aflatoxin-producing Aspergillus nomius. Mycologia 103:174–183

    PubMed  Google Scholar 

  • Horn BW, Olarte RA, Peterson SW, Carbone I (2013) Sexual reproduction in Aspergillus tubingensis from section Nigri. Mycologia 105:1153–1163

    CAS  PubMed  Google Scholar 

  • Horn BW, Ramirez-Prado J, Carbone I (2009b) The sexual state of Aspergillus parasiticus. Mycologia 101:275–280

    PubMed  Google Scholar 

  • Horn BW, Ramirez-Prado JH, Carbone I (2009c) Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticus. Fungal Genet Biol 46:169–175

    CAS  PubMed  Google Scholar 

  • Houbraken J, Frisvad JC, Seifert KA, Overy DP, Tuthill DM, Valdez JG, Samson RA (2012) New penicillin-producing Penicillium species and an overview of section Chrysogena. Persoonia 29:78–100

    PubMed Central  CAS  PubMed  Google Scholar 

  • Houbraken J, Varga J, Rico-Munoz E, Johnson S, Samson RA (2008) Sexual reproduction as the cause of heat resistance in the food spoilage fungus Byssochlamys spectabilis (anamorph Paecilomyces variotii). Appl Environ Microbiol 74:1613–1619

    PubMed Central  CAS  PubMed  Google Scholar 

  • Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Adv Appl Microbiol 86:199–249

    PubMed  Google Scholar 

  • Idnurm A (2011) Sex determination in the first-described sexual fungus. Eukaryot Cell 10:1485–1491

    PubMed Central  CAS  PubMed  Google Scholar 

  • ** Y, Allen S, Baber L, Bhattarai EK, Lamb TM, Versaw WK (2007) Rapid genetic map** in Neurospora crassa. Fungal Genet Biol 44:455–465

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jurgenson JE, Zeller KA, Leslie JF (2002) Expanded genetic map of Gibberella moniliformis (Fusarium verticillioides). Appl Environ Microbiol 68:1972–1979

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kawasaki M, Anzawa K, Wakasa A, Takeda K, Mochizuki T, Ishizaki H, Hemashettar B (2010) Matings among three teleomorphs of Trichophyton mentagrophytes. Jpn J Med Mycol 51:143–452

    CAS  Google Scholar 

  • Kent CR, Ortiz-Bermúdez P, Gilies SS, Hull CM (2008) Formulation of a defined V8 medium for induction of sexual development of Cryptococcus neoformans. Appl Environ Biol 74:6248–6253

    CAS  Google Scholar 

  • Kerényi Z, Moretti A, Waalwijk C, Olah B, Hornok L (2004) Mating type sequences in asexually reproducing Fusarium species. Appl Environ Microbiol 70:4419–4423

    PubMed Central  PubMed  Google Scholar 

  • Klittich CJR, Leslie JF (1988) Nitrate reduction mutants of Fusarium moniliforme (Gibberella fujikuroi). Genetics 118:417–423

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kwon-Chung KJ, Sugui JA (2009) Sexual reproduction in Aspergillus species of medical or economic importance: why so fastidious? Trends Microbiol 17:481–487

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kwon-Chung KJ, Weeks RJ, Larsh HW (1974) Studies on Emmonsiella capsulata (Histoplasma capsulatum). II. Distribution of the two mating types in 13 endemic states of the United States. Am J Epidemiol 99:44–49

    CAS  PubMed  Google Scholar 

  • Lambreghts R, Shi M, Belden WJ, deCaprio D, Park D, Henn MR, Galagan JE, Baştürkmen M, Birren BW, Sachs MS, Dunlap JC, Loros JL (2009) A high-density single nucleotide polymorphism map for Neurospora crassa. Genetics 181:467–781

    Google Scholar 

  • Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74:298–340

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lewis ZA, Shiver AL, Stiffler N, Miller MR, Johnson EA, Selker EU (2007) High-density detection of restriction-site-associated DNA markers for rapid map** of mutated loci in Neurospora. Genetics 177:1163–1171

    PubMed Central  CAS  PubMed  Google Scholar 

  • López-Villavicencio M, Aguileta G, Giraud T, de Vienne DM, Lacoste S, Couloux A, Dupont J (2010) Sex in Penicillium: combined phylogenetic and experimental approaches. Fungal Genet Biol 47:693–706

    PubMed  Google Scholar 

  • McAlpin CE, Wicklow DT (2005) Culture media and sources of nitrogen promoting the formation of stromata and ascocarps in Petromyces alliaceus (Aspergillus section Flavi). Can J Microbiol 51:765–771

    CAS  PubMed  Google Scholar 

  • Metzenberg RL, Glass NL (1990) Mating type and mating strategies in Neurospora. Bioessays 12:53–59

    CAS  PubMed  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (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 U S A 88:9828–9832

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miles CM, Wayne M (2008) Quantitative trait locus (QTL) analysis. Nat Educ 1:208

    Google Scholar 

  • Milgroom MG (1996) Recombination and the multilocus structure of fungal population. Annu Rev Phytopathol 34:457–477

    CAS  PubMed  Google Scholar 

  • Mooney JL, Yager LN (1990) Light is required for conidiation in Aspergillus nidulans. Genes Dev 4:1473–1482

    CAS  PubMed  Google Scholar 

  • Moore GG (2014) Sex and recombination in aflatoxigenic Aspergilli: global implications. Front Microbiol 5:32

    PubMed Central  PubMed  Google Scholar 

  • Murtagh GJ, Dyer PS, Crittenden PD (2000) Sex and the single lichen. Nature 404:564

    CAS  PubMed  Google Scholar 

  • Nielsen KA, De Obaldia AL, Heitman J (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6:949959

    Google Scholar 

  • Nowrousian M, Teichert I, Masloff S, Kück U (2012) Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3. Genes Genomes Genetics 2:261–270

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nováková A, Hubka V, Dudová Z, Matsuzawa T, Kubátová A, Yaguchi T, Kolařík M (2014) New species in Aspergillus section Fumigati from reclamation sites in Wyoming (U.S.A.) and revision of A. viridinutans complex. Fung Div 64(1):253–274. doi:10.1007/s13225-013-0262-5

    Google Scholar 

  • O’Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471–474

    PubMed  Google Scholar 

  • Paoletti M, Rydholm C, Schwier EU, Anderson MJ, Szakacs G, Lutzoni F, Debeaupuis JP, Latgé JP, Denning DW, Dyer PS (2005) Evidence for sexuality in the opportunistic human pathogen Aspergillus fumigatus. Curr Biol 15:1242–1248

    CAS  PubMed  Google Scholar 

  • Paoletti M, Seymour FA, Alcocer MJC, Kaur N, Calvo AM, Archer DB, Dyer PS (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 17:1384–1389

    CAS  PubMed  Google Scholar 

  • Perkins DD (1986) Hints and precautions for the care, feeding and breeding of Neurospora. Fungal Genet Newsl 33:36–41

    Google Scholar 

  • Pitt JI (1979) The genus Penicillium and its teleomorph states Eupenicillium and Talaromyces. Academic, London, UK

    Google Scholar 

  • Pöggeler S (2001) Mating-type genes for classical strain improvements of ascomycetes. Appl Microbiol Biotechnol 56:589–601

    PubMed  Google Scholar 

  • Pomraning KR, Smith KM, Freitag M (2011) Bulk segregant analysis followed by high-throughput sequencing reveals the Neurospora cell cycle gene, ndc-1, to be allelic with the gene for ornithine decarboxylase, spe-1. Eukaryot Cell 10:724–733

    Google Scholar 

  • Pringle A, Baker DM, Platt JL, Wares JP, Latgé JP, Taylor JW (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–1899

    CAS  PubMed  Google Scholar 

  • Raju NB, Perkins DD (1994) Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora and Podospora. Dev Genet 15:104–118

    CAS  PubMed  Google Scholar 

  • Ramirez-Prado JH, Moore GG, Horn BW, Carbone I (2008) Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticus. Fungal Genet Biol 45:1292–1299

    CAS  PubMed  Google Scholar 

  • Raper KB, Fennell DI (1965) The genus Aspergillus. Williams & Wilkins Co, Baltimore

    Google Scholar 

  • Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372

    PubMed  Google Scholar 

  • Robellet X, Oestreicher N, Guitton A, Vélot C (2010) Gene silencing of transgenes inserted in the Aspergillus nidulans alcM and/or alcS loci. Curr Genet 56:341–348

    CAS  PubMed  Google Scholar 

  • Ropars J, López-Villavicencio M, Dupont J, Snirc A, Gillot G, Coton M, Jany J-L, Coton E, Giraud T (2014) Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti. Evol Appl 7:433–441

    PubMed Central  PubMed  Google Scholar 

  • Rydholm C, Dyer PS, Lutzoni F (2007) DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell 6:868–874

    PubMed Central  CAS  PubMed  Google Scholar 

  • Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS laboratory manual Series 2. CBS KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands

    Google Scholar 

  • Samson RA, Varga J, Dyer PS (2009) Morphology and reproductive mode of Aspergillus fumigatus. In: Latgé JP, Steinbach WJ (eds) Aspergillus fumigatus and Aspergillosis. ASM, Washington, pp 7–13

    Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246

    PubMed Central  CAS  PubMed  Google Scholar 

  • Seidl V, Seibel C, Kubicek CP, Schmoll M (2009) Sexual development in the industrial workhorse Trichoderma reesei. Proc Natl Acad Sci U S A 106:13909–13914

    PubMed Central  CAS  PubMed  Google Scholar 

  • Seymour FA, Crittenden PD, Dickinson MJ, Paoletti M, Montiel D, Cho L, Dyer PS (2005) Breeding systems in the lichen-forming fungal genus Cladonia. Fungal Genet Biol 42:554–563

    CAS  PubMed  Google Scholar 

  • Short DP, O’Donnell K, Thrane U, Nielsen KF, Zhang N, Juba JH, Geiser DM (2013) Phylogenetic relationships among members of the Fusarium solani species complex in human infections and the descriptions of F. keratoplasticum sp. nov. and F. petroliphilum stat. nov. Fungal Genet. Biol 53:59–70

    Google Scholar 

  • Singh G, Dyer PS, Ashby AM (1999) Intra-specific and inter-specific conservation of mating-type genes from the discomycete plant-pathogenic fungi Pyrenopeziza brassicae and Tapesia yallundae. Curr Genet 36:290–300

    CAS  PubMed  Google Scholar 

  • Steenkamp ET, Wingfield BD, Coutinho TA, Zeller KA, Wingfield MJ, Marasas WF, Leslie JF (2000) PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Appl Environ Microbiol 66:4378–4382

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sugui JA, Losada L, Wang W, Varga J, Ngamskulrungroj P, Abu-Asab M, Chang YC, O'Gorman CM, Wickes BL, Nierman WC, Dyer PS, Kwon-Chung KJ (2011) Identification and characterization of an Aspergillus fumigatus “supermater” pair. MBio 2:e00234–11

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sugui JA, Vinh DC, Nardone G, Shea YR, Chang YC, Zelazny AM, Marr KA, Holland SM, Kwon-Chung KJ (2010) Neosartorya udagawae (Aspergillus udagawae), an emerging agent of aspergillosis: how different is it from Aspergillus fumigatus? J Clin Microbiol 48:220–228

    PubMed Central  CAS  PubMed  Google Scholar 

  • Swilaiman SS, O’Gorman CM, Balajee SA, Dyer PS (2013) Discovery of a sexual cycle in Aspergillus lentulus, a close relative of A. fumigatus. Eukaryot Cell 12:962–969

    PubMed Central  CAS  PubMed  Google Scholar 

  • Takada M, Udagawa S (1988) A new species of heterothallic Talaromyces. Mycotaxon 31:417–425

    Google Scholar 

  • Takan JP, Chipili J, Muthumeenakshi S, Talbot NJ, Manyasa EO, Bandyopadhyay R, Sere Y, Nutsugah SK, Talhinhas P, Hossain M, Brown AE, Sreenivasaprasad S (2012) Magnaporthe oryzae populations adapted to finger millet and rice exhibit distinctive patterns of genetic diversity, sexuality and host interaction. Mol Biotechnol 50:145–158

    CAS  PubMed  Google Scholar 

  • Todd RB, Davis MA, Hynes MJ (2007) Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2:811–821

    CAS  PubMed  Google Scholar 

  • Turner E, Jacobson DJ, Taylor JW (2011) Genetic architecture of a reinforced, postmating reproductive isolation barrier between Neurospora spceies indicates evolution via natural selection. PLoS Genet 7:e1002204

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tschanz AT, Horst RK, Nelson PE (1976) The effect of environment on sexual reproduction of Gibberella zeae. Mycologia 68:327–340

    Google Scholar 

  • Turgeon BG, Yoder OC (2000) Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31:1–5

    CAS  PubMed  Google Scholar 

  • Yoon J, Maruyama J, Kitamoto K (2011) Disruption of ten protease genes in the filamentous fungus Aspergillus oryzae highly improves production of heterologous proteins. Appl Microbiol Biotechnol 89:747–759

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

J.H. thanks Tineke van Doorn and Richard Summerbell for the discussions on the term proto-heterothallic.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jos Houbraken Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Houbraken, J., Dyer, P.S. (2015). Induction of the Sexual Cycle in Filamentous Ascomycetes. In: van den Berg, M., Maruthachalam, K. (eds) Genetic Transformation Systems in Fungi, Volume 2. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-10503-1_2

Download citation

Publish with us

Policies and ethics

Navigation