Skip to main content
SpringerLink
Log in

Genetics of Cordyceps and related fungi

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Ascomycete Cordyceps sensu lato consists of hundreds of species of fungi capable of infecting different insects. Species of these fungi are either valued traditional Chinese medicines or used for biocontrol of insect pests. Phylogenomic analysis indicated that fungal entomopathogenicity has evolved for multiple times, and the species of Cordyceps were diverged from the mycoparasite or plant endophyte. Relative to plant pathogens and saprophytes, Cordyceps species demonstrate characteristic genome expansions of proteases and chitinases that are used by the fungi to target insect cuticles. Only a single mating-type gene identified in the sequenced species of Cordyceps sensu lato indicates that these fungi are sexually heterothallic, but the gene structure of the mating-type loci and frequency in performing sexual cycle are considerably different between different species. Similar to the model fungus Neurospora crassa, Cordyceps and related fungi contain the full components for RNA interference pathways. However, the mechanism of repeat-induced point mutation varies between different fungi. Epigenetic rather than genetic alterations are majorly responsible for the frequent occurrence of culture degeneration in Cordyceps-related species. Future genetic and epigenetic studies of fungal sexuality controls and culture degeneration mechanisms will benefit the cost-effective applications of Cordyceps and related fungi in pharmaceuticals and agriculture.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alby K, Schaefer D, Bennett RJ (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 480(7257):890–893

    Article  Google Scholar 

  • Chang SS, Zhang Z, Liu Y (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305–323

    Article  CAS  Google Scholar 

  • Colombo D, Ammirati E (2011) Cyclosporine in transplantation—a history of converging timelines. J Biol Regul Homeost Agents 25(4):493–504

    CAS  Google Scholar 

  • Cuomo CA, Güldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang YL, Decaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes HW, Mitterbauer R, Muehlbauer G, Münsterkötter M, Nelson D, O'donnell K, Ouellet T, Qi W, Quesneville H, Roncero MI, Seong KY, Tetko IV, Urban M, Waalwijk C, Ward TJ, Yao J, Birren BW, Kistler HC (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–1402

    Article  CAS  Google Scholar 

  • de Faria MR, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256

    Article  Google Scholar 

  • Douma RD, Batista JM, Touw KM, Kiel JA, Krikken AM, Zhao Z, Veiga T, Klaassen P, Bovenberg RA, Daran JM, Heijnen JJ, van Gulik WM (2011) Degeneration of penicillin production in ethanol-limited chemostat cultivations of Penicillium chrysogenum: a systems biology approach. BMC Syst Biol 5:132

    Article  CAS  Google Scholar 

  • Duan ZB, Shang YF, Gao Q, Zheng P, Wang CS (2009) A phosphoketolase Mpk1 of bacterial origin is adaptively required for full virulence in the insect-pathogenic fungus Metarhizium anisopliae. Environ Microbiol 11(9):2351–2360

    Article  CAS  Google Scholar 

  • Dyer PS, O'Gorman CM (2012) Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol Rev 36(1):165–192

    Article  CAS  Google Scholar 

  • Fang WG, Azimzadeh P, St Leger RJ (2012) Strain improvement of fungal insecticides for controlling insect pests and vector-borne diseases. Curr Opin Microbiol 15(3):232–238

    Article  Google Scholar 

  • Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20(9):417–423

    Article  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868

    Article  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Bastürkmen 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 BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115

    Article  CAS  Google Scholar 

  • Gao Q, Jin K, Ying SH, Zhang YJ, Xiao GH, Shang YF, Duan ZB, Hu X, Xie XQ, Zhou G, Peng GX, Luo ZB, Huang W, Wang B, Fang WG, Wang SB, Zhong Y, Ma LJ, St. Leger RJ, Zhao GP, Pei Y, Feng MG, Xia YX, Wang CS (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7(1):1001264

  • Hejtmanek M, Hejtmankova N (1989) Teleomorphs and mating types in Trichophyton mentagrophytes complex. Acta Univ Palacki Olomuc Fac Med 123:11–33

    CAS  Google Scholar 

  • Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 50:213–257

    Article  CAS  Google Scholar 

  • Idnurm A (2011) Sex and speciation: the paradox that non-recombining DNA promotes recombination. Fungal Biol Rev 25(3):121–127

    Article  Google Scholar 

  • Keyhani N (2011) Fungal genomes and beyond. Fungal Genom Biol 1:e101

    Google Scholar 

  • Kikot GE, Hours RA, Alconada TM (2009) Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review. J Basic Microbiol 49(3):231–241

    Article  CAS  Google Scholar 

  • Kim DH (1997) Induced change in DNA methylation of Fusarium oxysporum f. sp. niveum due to successive transfer. J Biochem Mol Biol 30:216–221

    CAS  Google Scholar 

  • Klix V, Nowrousian M, Ringelberg C, Loros JJ, Dunlap JC, Pöggeler S (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(6):894–905

    Article  CAS  Google Scholar 

  • Kronstad JW, Staben C (1997) Mating type in filamentous fungi. Annu Rev Genet 31:245–276

    Article  CAS  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(2):298–340

    Article  CAS  Google Scholar 

  • Leng YJ, Peng GX, Cao YQ, Xia YX (2011) Genetically altering the expression of neutral trehalase gene affects conidiospore thermotolerance of the entomopathogenic fungus Metarhizium acridum. BMC Microbiol 11:32

    Article  CAS  Google Scholar 

  • Li A, Begin M, Kokurewicz K, Bowden C, Horgen PA (1994) Inheritance of strain instability (sectoring) in the commercial button mushroom, Agaricus bisporus. Appl Environ Microbiol 60:2384–2388

    CAS  Google Scholar 

  • Li ZZ, Li CR, Huang B, Fan MZ (2001) Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomogenous fungus. Chinese Sci Bull 46:751–753

    Article  Google Scholar 

  • Li L, Pischetsrieder M, St Leger RJ, Wang CS (2008) Associated links among mtDNA glycation, oxidative stress and colony sectorization in Metarhizium anisopliae. Fungal Genet Biol 45:1300–1306

    Article  CAS  Google Scholar 

  • Li ZZ, Alves SB, Roberts DW, Fan M, Delalibera I Jr, Tang J, Lopes RB, Faria M, Rangel DEN (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Technol 20:117–136

    Article  Google Scholar 

  • Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373

    Article  CAS  Google Scholar 

  • Magae Y, Akahane K, Nakamura K, Tsunoda S (2005) Simple colorimetric method for detecting degenerate strains of the cultivated basidiomycete Flammulina velutipes (Enokitake). Appl Environ Microbiol 71:6388–6389

    Article  CAS  Google Scholar 

  • Meyling NV, Lübeck M, Buckley EP, Eilenberg J, Rehner SA (2009) Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol Ecol 18(6):1282–1293

    Article  CAS  Google Scholar 

  • Molnár I, Gibson DM, Krasnoff SB (2010) Secondary metabolites from entomopathogenic Hypocrealean fungi. Nat Prod Rep 27(9):1241–1275

    Article  Google Scholar 

  • Ni M, Feretzaki M, Sun S, Wang X, Heitman J (2011) Sex in fungi. Annu Rev Genet 45:405–430

    Article  CAS  Google Scholar 

  • Nygren K, Strandberg R, Wallberg A, Nabholz B, Gustafsson T, García D, Cano J, Guarro J, Johannesson H (2011) A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol Phylogenet Evol 59(3):649–663

    Article  Google Scholar 

  • Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, Klein F (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146(3):372–383

    Article  CAS  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 fungal pathogen Aspergillus fumigatus. Curr Biol 15(13):1242–1248

    Article  CAS  Google Scholar 

  • Paterson RR (2008) Cordyceps: a traditional Chinese medicine and another fungal therapeutic biofactory? Phytochemistry 69:1469–1495

    Article  CAS  Google Scholar 

  • Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100(2):205–226

    Article  CAS  Google Scholar 

  • Pöggeler S, Kück U (2000) Comparative analysis of the mating-type loci from Neurospora crassa and Sordaria macrospora: identification of novel transcribed ORFs. Mol Gen Genet 263(2):292–301

    Article  Google Scholar 

  • Rohlfs M, Churchill AC (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48(1):23–34

    Article  CAS  Google Scholar 

  • Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353

    Article  CAS  Google Scholar 

  • Ryan MJ, Bridge PD, Smith D, Jeffries P (2002) Phenotypic degeneration occurs during sector formation in Metarhizium anisopliae. J Appl Microbiol 93:163–168

    Article  CAS  Google Scholar 

  • Schmidt HA, Petzold E, Vingron M, von Haeseler A (2003) Molecular phylogenetics: parallelized parameter estimation and quartet puzzling. J Parallel Distrib Comput 63:719–727

    Article  Google Scholar 

  • Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46:439–450

    Article  CAS  Google Scholar 

  • St. Leger RJ, Wang CS (2010) Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl Microbiol Biotechnol 85:901–907

    Article  CAS  Google Scholar 

  • St. Leger RJ, Wang CS, Fang WG (2011) New perspectives on insect pathogens. Fungal Biol Rev 25:84–88

    Article  Google Scholar 

  • Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59

    Article  Google Scholar 

  • Sung GH, Poinar GO Jr, Spatafora JW (2008) The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Mol Phylogenet Evol 49(2):495–502

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Wang CS, Skrobek A, Butt TM (2003) Concurrence of losing a chromosome and the ability to produce destruxins in a mutant of Metarhizium anisopliae. FEMS Microbiol Lett 226:373–378

    Article  CAS  Google Scholar 

  • Wang CS, Skrobek A, Butt TM (2004) Investigations on the destruxin production of the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 85:168–174

    Article  CAS  Google Scholar 

  • Wang CS, Butt TM, St. Leger RJ (2005) Colony sectorization of Metarhizium anisopliae is a sign of ageing. Microbiology (UK) 151(10):3223–3236

    Article  CAS  Google Scholar 

  • Wang CS, Duan ZB, St Leger RJ (2008) MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryot Cell 7(2):302–309

    Article  Google Scholar 

  • Wang SB, O'Brien TR, Pava-Ripoll M, St Leger RJ (2011) Local adaptation of an introduced transgenic insect fungal pathogen due to new beneficial mutations. Proc Natl Acad Sci USA 108(51):20449–20454

    Article  CAS  Google Scholar 

  • White S, McIntyre M, Berry DR, McNeil B (2002) The autolysis of industrial filamentous fungi. Crit Rev Biotechnol 22(1):1–14

    Article  Google Scholar 

  • Whittle CA, Nygren K, Johannesson H (2011) Consequences of reproductive mode on genome evolution in fungi. Fungal Genet Biol 48(7):661–667

    Article  CAS  Google Scholar 

  • Xiao JH, Zhong JJ (2007) Secondary metabolites from Cordyceps species and their antitumor activity studies. Recent Pat Biotechnol 1:123–137

    Article  CAS  Google Scholar 

  • Xiao GH, Ying SH, Zheng P, Wang ZL, Zhang SW, Xie XQ, Shang YF, St. Leger RJ, Zhao GP, Wang CS, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483

    Google Scholar 

  • Xiong CH, Xia YL, Zheng P, Wang CS (2013) Increasing oxidative stress tolerance and subculturing stability of Cordyceps militaris by overexpression of a glutathione peroxidase gene. Appl Microbiol Biotechnol 97:2009–2015

    Google Scholar 

  • Yokoyama E, Arakawa M, Yamagishi K, Hara A (2006) Phylogenetic and structural analyses of the mating-type loci in Clavicipitaceae. FEMS Microbiol Lett 264(2):182–191

    Article  CAS  Google Scholar 

  • Zheng P, Xia Y, Xiao G, Xiong C, Hu X, Zhang S, Zheng H, Huang Y, Zhou Y, Wang S, Zhao GP, Liu X, St Leger RJ, Wang CS (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12:R116

    Article  CAS  Google Scholar 

  • Zhou X, Gong Z, Su Y, Lin J, Tang K (2009) Cordyceps fungi: natural products, pharmacological functions and developmental products. J Pharm Pharmacol 61:279–291

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Natural Science Foundation of China (30970034) and the Science and Technology Commission of Shanghai Municipality (Grant No. 08DZ1970200).

Author information

Authors and Affiliations

  1. Key Laboratory of Insect Developmental and Evolutionary Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China

    Peng Zheng, Yongliang Xia, Siwei Zhang & Chengshu Wang

Authors
  1. Peng Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongliang Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chengshu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chengshu Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zheng, P., Xia, Y., Zhang, S. et al. Genetics of Cordyceps and related fungi. Appl Microbiol Biotechnol 97, 2797–2804 (2013). https://doi.org/10.1007/s00253-013-4771-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-4771-7

Keywords

Search

Navigation