Abstract
The sexual cycle offers valuable opportunities to study and modify fungal gene expression. However, exploitation of sexual reproduction has often been overlooked because many fungal species of importance in biotechnology, medicine and agriculture lack a sexual cycle, and therefore gene manipulation techniques have been used in preference to sex. It has been discovered in the last decade though that many supposedly asexual species have the potential for sexual development if the correct environmental conditions and mating partners can be identified. This has led to renewed interest in experimental exploitation of fungal sexual cycles. An overview of fungal sexual reproduction is first provided. We then describe a series of ways in which fungal sexual cycles can be used to study and modify gene expression systems. These include the use of sexual reproduction in determining the genetic basis of traits of interest, use in identification of candidate genes, use in industrial strain development, and verification of gene function in deletion and complementation studies. Finally the use of mating-type (MAT) genes to enhance expression of desirable traits relating to primary and secondary metabolism is discussed, given recent finding about their wide-ranging transcriptional activity.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Becker K, Beer C, Freitag M, Kück U. Genome-wide identification of target genes of a mating-type α-domain transcription factor reveals functions beyond sexual development. Mol Microbiol. 2015;96:1002–22. doi:10.1111/mmi.12987.
Böhm J, Hoff B, O’Gorman CM, Wolfers S, Klix V, Binger D, et al. Sexual reproduction and mating-type-mediated strain development in the penicillin-producing fungus Penicillium chrysogenum. Proc Natl Acad Sci U S A. 2013;110:1476–81. doi:10.1073/pnas.1217943110.
Böhm J, Dahlmann TA, Gümüser H, Kück U. A MAT1-2 wild- type strain from Penicillium chrysogenum: functional mating- type locus characterization, genome sequencing and mating with an industrial penicillin-producing strain. Mol Microbiol. 2015;95:859–74. doi:10.1111/mmi.12909.
Burdock GA, Flamm WG. Safety assessment of the mycotoxin cyclopiazonic acid. Int J Toxicol. 2000;19:195–218. doi:10.1080/10915810050074964.
Cavindera B, Trail F. Role of Fig1, a component of the low-affinity calcium uptake system, in growth and sexual development of filamentous fungi. Eukaryot Cell. 2012;11:978–88. doi:10.1128/EC.00007-12.
Dahlmann TA, Böhm J, Becker K, Kück U. Sexual recombination as a tool for engineering industrial Penicillium chrysogenum strains. Curr Genet. 2015;61:679–83. doi:10.1007/s00294-015-0497-7.
Debuchy R, Berteaux-Lecellier V, Silar P. Mating systems and sexual morphogenesis in Ascomycetes. In: Borkovitch K, Ebbole D, editors. Cellular and Molecular Biology of Filamentous Fungi. Washington, DC: ASM Press; 2010. p. 501–35.
Dyer PS, Darbyshir H. Utilisation of the sexual cycle in filamentous fungi as a tool for gene identification, strain improvement and gene manipulation. Fungal Biol Rev. 2016 (manuscript under review).
Dyer PS, Inderbitzin P, Debuchy R. Mating-type structure, function, regulation and evolution in the Pezizomycotina. In: Wendland J, editor. The Mycota, vol. XIV. Berlin: Springer; 2015 (In press).
Dyer PS, O’Gorman CM. A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol. 2011;14:649–54. doi:10.1016/j.mib.2011.10.001.
Dyer PS, O’Gorman CM. Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol Rev. 2012;36:165–92. doi:10.1111/j.1574-6976.2011.00308.x.
Dyer PS, Paoletti M. Reproduction in Aspergillus fumigatus: sexuality in a supposedly asexual species? Med Mycol. 2005;43:S7–14. doi:10.1080/13693780400029015.
Dyer PS, Ingram DS, Johnstone K. The control of sexual morphogenesis in the Ascomycotina. Biol Rev. 1992;67:421–58. doi:10.1111/j.1469-185X.1992.tb01189.x.
Dyer PS, Hansen J, Delaney A, Lucas JA. Genetic control of resistance to the sterol 14α-demethylase inhibitor fungicide prochloraz in the cereal eyespot pathogen Tapesia yallundae. Appl Environ Microbiol. 2000;66:4599–604. doi:10.1128/AEM.66.11.4599-4604.2000..
Fell JW, Boekhout T, Fonseca A, Sampaio JP. Basidiomycetous yeasts. In: McLaughlin DJ, McLaughlin EG, Lemke PA, editors. The Mycota, Systematics and Evolution, vol. VII, Part B. Berlin: Springer; 2001. p. 1–36.
Foulongne-Oriol M. Genetic linkage mapping in fungi: current state, applications, and future trends. Appl Microbiol Biot. 2012;95:891–904. doi:10.1007/s00253-012-4228-4.
Fraser JA, Heitman J. Fungal mating-type loci. Curr Biol. 2003;13:792–5. doi:10.1016/j.cub.2003.09.046.
Frisvad JC, Petersen LM, Lyhne EK, Larsen TO. Formation of sclerotia and production of indoloterpenes by Aspergillus niger and other species in section Nigri. PLoS One. 2014;9, e94857. doi:10.1371/journal.pone.0094857.
Grognet P, Bidard F, Kuchly C, Tong LC, Coppin E, Benkhali JA. Maintaining two mating types: structure of the mating type locus and its role in heterokaryosis in Podospora anserina. Genetics. 2014;197:421–32. doi:10.1534/genetics.113.159988.
Hall C. Quantitative genetics in Neurospora. In: Kasbekar DP, McCluskey K, editors. Neurospora Genomics and Molecular Biology. Norfolk: Caister Academic Press; 2013. p. 65–84.
Hamamoto H, Hasegawa K, Nakaune R, Lee YJ, Makizumi Y, Akutsu K, et al. Tandem repeat of a transcriptional enhancer upstream of the sterol 14α-demethylase gene (CYP51) in Penicillium digitatum. Appl Environ Microbiol. 2000;66:3421–6. doi:10.1128/AEM.66.8.3421-3426.2000.
Heitman JH, Kronstad JW, Taylor JW, Casselton LA. Sex in Fungi – Molecular Determination and Evolutionary Implications. Washington: ASM Press; 2007.
Horn BW, Ramirez-Prado JH, Carbone I. Sexual reproduction and recombination in the aflatoxin producing fungus Aspergillus parasiticus. Fungal Genet Biol. 2009;46:169–75. doi:10.1016/j.fgb.2008.11.004.
Houbraken J, Dyer PS. Induction of the sexual cycle in filamentous Ascomycetes. In: van den Berg MA, Maruthachalam K, editors. Genetic transformation systems in fungi, vol. 2. Berlin: Springer; 2015. p. 23–45. doi:10.1007/978-3-319-10503-1.
Knight SC, Anthony VM, Brady AM, Greenland AJ, Heaney SP, Murray DC, et al. Rationale and perspectives on the development of fungicides. Annu Rev Phytopathol. 1997;35:349–72. doi:10.1146/annurev.phyto.35.1.349.
Kretschmer M, Leroch M, Mosbach A, Walker AS, Fillinger MD, et al. Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathogens. 2009;5:e1000696. doi:10.1371/journal.ppat.1000696.
Ma Z, Michailides TJ. Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Protect. 2005;24:853–63. doi:10.1016/j.cropro.2005.01.011.
Martin T, Lu SW, van Tilbeurgh H, Ripoll DR, Dixelius C, Turgeon BG, Debuchy R. Tracing the origin of the fungal α1 domain places its ancestor in the HMG-box superfamily: implications for fungal mating-type evolution. PLoS One. 2010;5, e15199. doi:10.1371/journal.pone.0015199.
Metzenberg RL, Glass NL. Mating type and mating strategies in Neurospora. Bioessays. 1990;12:53–9.
Michelmore RW, Paran I, Kesseli RV. 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. 1991;88:9828–32. doi:10.1073/pnas.88.21.9828.
Miles CM, Wayne M. Quantitative trait locus (QTL) analysis. Nat Educ. 2008;1:208.
Moore D, Novak Frazer LA. Essential fungal genetics. New York: Springer-Verlag; 2002.
Nowrousian M, Teichert I, Masloff S, Kück U. Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3, Genes, Genomes. Genetics. 2012;2:261–70. doi:10.1534/g3.111.001479.
O’Gorman CM, Fuller HT, Dyer PS. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature. 2009;457:471–4. doi:10.1038/nature07528.
Olarte RA, Horn BW, Dorner JW, Monacell JT, Singh R, Stone EA, et al. Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Mol Ecol. 2012;21:1453–76. doi:10.1111/j.1365-294X.2011.05398.x.
Paoletti M, Seymour FA, Alcocer MJ, Kaur N, Calvo AM, Archer DB, et al. Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol. 2007;17:1384–9. doi:10.1016/j.cub.2007.07.012.
Pöggeler S, Masloff S, Jacobsen S, Kück U. Karyotype polymorphism correlates with intraspecific infertility in the homothallic ascomycete Sordaria macrospora. J Evol Biol. 2000;13:281–9. doi:10.1046/j.1420-9101.2000.00174.x.
Pomraning KR, Smith KM, Freitag M. 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. 2011;10:724–33. doi:10.1128/EC.00016-11.
Rieseberg LH, Archer MA, Wayne RK. Transgressive segregation, adaption and speciation. Heredity. 1999;83:363–72. doi:10.1038/sj.hdy.6886170.
Ropars J, López-Villavicencio M, Dupont J, Snirc A, Gillot G, Coton M, Jany J, Coton E, Giraud T. Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti. Evol Appl. 2014;7:433–41. doi:10.1111/eva.12140.
Seidl V, Seribel C, Kubicek CP, Schmoll M. Sexual development in the industrial workhorse Trichoderma reesei. Proc Natl Acad Sci U S A. 2009;106:13909–14. doi:10.1073/pnas.0904936106.
Swilaiman SS. Sexual potential and population biology of fungal Aspergillus and Penicillium species. Ph.D. Thesis. Nottingham: University of Nottingham; 2013.
Serna L, Stadler D. Nuclear division cycle in germinating conidia of Neurospora crassa. J Bacteriol. 1978;136:341–51.
Todd RB, Davis MA, Hynes MJ. Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc. 2007;2:811–21. doi:10.1038/nprot.2007.112.
Vitalini MW, Morgan LW, March IJ, Bell-Pedersen D. A genetic selection for circadian output pathway mutations in Neurospora crassa. Genetics. 2004;167:119–29. doi:10.1534/genetics.167.1.119.
Wood HM, Dickinson MJ, Lucas JA, Dyer PS. Cloning of the CYP51 gene from the eyespot pathogen Tapesia yallundae indicates that resistance to the DMI fungicide prochloraz is not related to sequence changes in the gene encoding the target site enzyme. FEMS Microbiol Lett. 2001;196:183–7. doi:10.1111/j.1574-6968.2001.tb10562.x.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Ashton, G.D., Dyer, P.S. (2016). Sexual Development in Fungi and Its Uses in Gene Expression Systems. In: Schmoll, M., Dattenböck, C. (eds) Gene Expression Systems in Fungi: Advancements and Applications. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-27951-0_15
Download citation
DOI: https://doi.org/10.1007/978-3-319-27951-0_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-27949-7
Online ISBN: 978-3-319-27951-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)