Skip to main content
Log in

Characterization of mating-type idiomorphs suggests that Morchella importuna, Mel-20 and M. sextelata are heterothallic

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Morels (Morchella spp.) are highly prized for their culinary qualities and intensively collected worldwide by mycophiles. Morels are divided into three clades by phylogenetic analyses: black morels, yellow morels and the rufobrunnea clade. Morchella importuna, Mel-20 and M. sextelata are included in the black morel clade and are widely distributed in Yunnan province, China. M. importuna and M. sextelata have been artificially cultured in recent years, but their life cycles and reproductive systems are still poorly understood, which delays the progress of morel cultivation. In this study, the genomes of two ascospore isolates of M. importuna with opposite mating-type were sequenced and two idiomorphs, MAT1–1 and MAT1–2, were identified. The MAT1–2 idiomorph was 6.7 kb in length containing a single MAT1–2-1 gene, and the MAT1–1 idiomorph was 10.5 kb containing a MAT1–1-1 gene and two other open reading frames (ORFs), GME3123 and GME3124. These ORFs differed greatly from the homologues of previously published mating-type genes; therefore, we speculate that they are novel mating genes found only in morels. Single-ascospore populations of M. importuna, M. sextelata and Mel-20 were analysed, and the result indicated that the ratios of MAT1–1- and MAT1–2-harbouring idiomorphs were not significantly different from a 1:1 ratio. The results suggest that these three black morels are heterothallic.

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

Access this article

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

  • Belfiori B, Riccioni C, Paolocci F, Rubini A (2013) Mating type locus of Chinese black truffles reveals heterothallism and the presence of cryptic species within the T. indicum species complex. PLoS ONE 8(12):e82353

    Article  PubMed  PubMed Central  Google Scholar 

  • Belfiori B, Riccioni C, Paolocci F, Rubini A (2016) Characterization of the reproductive mode and life cycle of the whitish truffle Tuber borchii. Mycorrhiza 26:515–527

    Article  CAS  PubMed  Google Scholar 

  • Buscot F (1994) Ectomycorrhizal types and endobacteria associated with ectomycorrhizas of Morchella elata (Fr.) Boudier with Picea abies (L.) karst. Mycorrhiza 4:223–232

    Article  Google Scholar 

  • Chilvers MI, Jones S, Meleca J, Peever TL, Pethybridge SJ, Hay FS (2014) Characterization of mating type genes supports the hypothesis that Stagonosporopsis chrysanthemi is homothallic and provides evidence that Stagonosporopsis tanaceti is heterothallic. Currr Genet 60:295–302

    Article  CAS  Google Scholar 

  • Coppin E, Debuchy R, Arnaise S, Picard M (1997) Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol Biol Rev 61:411–428

    CAS  Google Scholar 

  • Debuchy R, Turgeon BG (2006) Mating-type structure, evolution, and function in Euascomycetes. The Mycota 1:293–323

    Article  CAS  Google Scholar 

  • Dodge BO (1920) The life history of Ascobolus magnificus. Mycologia 12:115–134

    Article  Google Scholar 

  • Du XH, Zhao Q, O’Donnell K, Rooney AP, Yang ZL (2012) Multigene molecular phylogenetics reveals true morels (Morchella) are especially species-rich in China. Fungal Genet Biol 49:455–469

    Article  CAS  PubMed  Google Scholar 

  • Du XH, Zhao Q, Yang ZL (2014) Diversity, evolutionary history and cultivation of morels: a review. Mycosystema 33:183–197

    CAS  Google Scholar 

  • Ferris JP, Pavlovic C, Fabry S, Goodenough UW (1997) Rapid evolution of sex-related genes in Chlamydomonas. Proc Natl Acad Sci U S A 94:8634–8639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira AVB, Saupe S, Glass NL (1996) Transcriptional analysis of the mt A idiomorph of Neurospora crassa identifies two genes in addition to mt A-1. Mol Gen Genet 250:767–774

    CAS  PubMed  Google Scholar 

  • Fu LH, Wang YP, Wang JJ, Yang YR, Hao LM (2013) Evaluation of the antioxidant activity of extracellular polysaccharides from Morchella esculenta. Food Funct 4:871–879

    Article  CAS  PubMed  Google Scholar 

  • Glass NL, Vollmer SJ, Staben C, Grotelueschen J, Metzenberg RL, Yanofsky C (1988) DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science 241:570–573

    Article  CAS  PubMed  Google Scholar 

  • Hervey A, Bistis G, Leong I (1978) Cultural studies of single ascospore isolates of Morchella esculenta. Mycologia 70:1269–1274

    Article  Google Scholar 

  • Hu M, Chen Y, Wang C, Cui H, Duan P, Zhai T, Yang Y, Li S (2013) Induction of apoptosis in HepG2 cells by polysaccharide MEP-II from the fermentation broth of Morchella esculenta. Biotechnol Lett 35:1–10

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson MI, Powell AJ, Tsang A, O’Toole N, Berka RM, Barry K, Grigoriev IV, Natvig DO (2016) Genetics of mating in members of the Chaetomiaceae as revealed by experimental and genomic characterization of reproduction in Myceliophthora heterothallica. Fungal Genet Biol 86:9–19

    Article  CAS  PubMed  Google Scholar 

  • Lu YZ, Xia YL, Luo FF, Dong CH, Wang CS (2016) Functional convergence and divergence of mating-type genes fulfilling in Cordyceps militaris. Fungal Genet Biol 88:35–43

    Article  CAS  PubMed  Google Scholar 

  • Masaphy S (2010) Biotechnology of morel mushrooms: successful fruiting body formation and development in a soilless system. Biotechnol Lett 32:1523–1527

    Article  CAS  PubMed  Google Scholar 

  • Martin SH, Wingfied BD, Wingfield MJ, Steenkamp ET (2011) Structure and evolution of Fusarium mating type locus: new insights from the Gibberella fujikuroi complex. Fungal Genet Biol 48:731–740

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miller SC(2005) Cultivation of Morchella US Patent 6,907,691

  • Nelson MA (1996) Mating systems in ascomycetes: aromp in the sac. Trends Genet 12:53–59

    Article  Google Scholar 

  • O’Donnell K, Rooney AP, Mills GL, Kuo M, Weber NS, Rehner SA (2011) Phylogeny and historical biogeography of true morels (Morchella) reveals an early cretaceous origin and high continental endemism and provincialism in the Holarctic. Fungal Genet Biol 48:252–265

    Article  PubMed  Google Scholar 

  • Ower R, Mills GL, Malachowski JA(1986) Cultivation of Morchella. US patent 4594809

  • Pagliaccia D, Douhan GW, Douhan LA, Peever TL, Carris LM, Kerrigan JL (2011) Development of molecular markers and preliminary investigation of the population structure and mating system in one lineage of black morel (Morchella elata) in the Pacific northwestern USA. Mycologia 103:969–982

    Article  CAS  PubMed  Google Scholar 

  • Peng WH, Tang J, He XL, Chen Y, Tang H (2016) Status analysis of artificial cultivation of Morchella in Sichuan(Chinese). Edible Med Mush 24:145–150

    CAS  Google Scholar 

  • Pildain MB, Visnovsky SB, Barroetavena C (2014) Phylogenetic diversity of true morels (Morchella),the main edible non-timber product from native Patagonian forests of Argentina. Fungal Biol 118:755–763

    Article  PubMed  Google Scholar 

  • Pilz D, McLain R, Alexander S, Villarreal-Ruiz Berch S, Wurtz TL, Parks CG, McFarlane E, Baker B, Molina R, Smith JE (2007) Ecology and Management of Morels Harvested from the Forests of Western North America. Gen Tech Rep PNW-GTR-710. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland

  • Pöggeler S (1999) Phylogenetic relationships between mating-type sequences from homothallic and heterothallic ascomycetes. Curr Genet 36:222–231

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Richard F, Bellanger JM, Clowez P, Hansen K, O’Donnell K, Urban A, Sauve M, Courtecuisse R, Moreau PA (2015) True morels (Morchella, Pezizales) of Europe and North America: evolutionary relationships inferred from multilocus data and a unified taxonomy. Mycologia 107:359–382

    Article  PubMed  Google Scholar 

  • Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci F (2011) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189:710–722

    Article  CAS  PubMed  Google Scholar 

  • Shear CL, Dodge BO (1927) Life histories and heterothallism of the red bread mould fungi of the Monillia sitipholia group. J Agric Res 34:1019–1042

    Google Scholar 

  • Su CA, Xu XY, Liu DY, Wu M, Zeng FQ, Zeng MY, Wei W, Jiang N, Luo X (2013) Isolation and characterization of exopolysaccharide with immunomodulatory activity from fermentation broth of Morchella conica. Daru J Pharmaceuti Sci 21:5

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Volk TJ, Leonard TJ (1990) Cytology of the life-cycle of Morchella. Mycol Res 94:399–406

    Article  Google Scholar 

  • Whitfield S, Lovell-Badge R, Goodfellow NP (1993) Rapid sequence evolution of the mammalian sex-determing gene SRY. Nature 364:713–715

    Article  CAS  PubMed  Google Scholar 

  • Wilken PM, Steenkamp ET, Hall TA, De Beer ZW, Wingfield MJ, Wingfield BD (2012) Both mating types in the heterothallic fungus Ophiostoma quercus contain MAT1-1 and MAT1-2 genes. Fungal Biol 116:427–437

    Article  CAS  PubMed  Google Scholar 

  • Whiterhouse HLK (1949) Heterothallism and sex in the fungi. Biol Rev 24:411–447

    Article  Google Scholar 

  • Xu LS, Jardini TM, Chen WD (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation Program of PR China (31460014) and the China Agriculture Research System (CARS-24).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yongchang Zhao.

Additional information

Section Editor: Eckhard Thines

Electronic supplementary material

Table S1

(DOCX 55 kb)

Table S2

(DOCX 21 kb)

Table S3

(DOCX 24 kb)

Figure S1

Maximum parsimonious phylograms (MP) of Elata Clade (black morels) inferred from combined analysis of ITS, RPB2, and TEF1 sequences from 36 collections. Grey highlight is used to point out that the strain in this study appears to be nested within the corresponding phylogenetically distinct species. The other 31 collections were reported in Du et al.(2012) and O’Donnell et al.(2011) (Supplementary Table S1). Sequences of M. rufobrunnea were used to root the phylogram. The number of each internode (above 60%) represents the MP bootstrap value based on1000 replicates of the data. (JPEG 3571 kb)

Figure S2

Maximum parsimonious phylograms (MP) of Esculenta Clade (yellow morels) inferred from combined analysis of ITS, TEF1 and LSU sequences from 44 collections. Grey highlight is used to point out that strain YAAS2689 appears to be nested within the corresponding phylogenetically distinct species Mes-15. The other 43 collections were reported in Du et al.(2012) and O’Donnell et al.(2011)(Supplementary Table S1). Sequences of M. rufobrunnea were used to root the phylogram. The number of each internode (above 60%) represents the MP bootstrap value based on1000 replicates of the data. (JPEG 1272 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chai, H., Chen, L., Chen, W. et al. Characterization of mating-type idiomorphs suggests that Morchella importuna, Mel-20 and M. sextelata are heterothallic. Mycol Progress 16, 743–752 (2017). https://doi.org/10.1007/s11557-017-1309-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-017-1309-x

Keywords

Navigation