Skip to main content
SpringerLink
Log in

Slow-growing heterokaryons as potential intermediates in supernumerary chromosome transfer between biotypes of Colletotrichum gloeosporioides

  • Short Communication
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

The vegetative transfer of a supernumerary chromosome between two biotypes (A and B) of Colletotrichum gloeosporioides pathogenic on Stylosanthes spp. has been previously demonstrated. The mechanism of transfer is unknown, and transient heterokaryosis has been implicated as an intermediary step, but inter-biotype heterokaryons have not so far been isolated. Conidia of a hygromycin-resistant strain of biotype A and a phleomycin-resistant strain of biotype B were mixed, co-cultured and plated on media containing both antibiotics and extremely slow-growing colonies resistant to both antibiotics isolated using repeated hyphal tip sub-culturing. Mononucleate conidia derived from these colonies were unable to germinate on media containing both antibiotics, but were able to germinate on media containing only one antibiotic, with hygromycin-resistant colonies predominating, indicating that unbalanced heterokaryons had formed. The heterokaryons had highly impaired growth rates suggesting some incompatibility. DNA marker analysis confirmed their heterokaryon status. These results demonstrate that unfit inter-biotype heterokaryons can form and potentially provide an intermediate step for supernumerary chromosomal exchange.

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

References

  • Akagi Y, Akamatsu H, Otani H, Kodama M (2009) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant pathogenic fungus. Eukaryot Cell 8:1732–1738

    Article  PubMed  CAS  Google Scholar 

  • Chacko RJ, Weidemann GJ, Tebeest DO, Correll JC (1994) The use of vegetative compatibility and heterokaryosis to determine potential genetic exchange in Colletotrichum gloeosporioides. Biol Control 4:382–389

    Article  Google Scholar 

  • Covert SF (1998) Supernumerary chromosomes in filamentous fungi. Curr Genet 33:311–319

    Article  PubMed  CAS  Google Scholar 

  • Glass NL, Dementhon K (2006) Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9:553–558

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Liu X, Benny U, Kistler HC, VanEtten HD (2001) Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 25:305–314

    Article  PubMed  CAS  Google Scholar 

  • Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A, Yamamoto M, Akimitsu K, Tsuge T (2002) A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59–70

    PubMed  CAS  Google Scholar 

  • He C, Masel AM, Irwin JAG, Kelemu S, Manners JM (1996) CgT1: a non-LTR retrotransposon with restricted distribution in the fungal phytopathogen Colletotrichum gloeosporioides. Mol Gen Genet 252:320–331

    PubMed  CAS  Google Scholar 

  • He C, Poplawski AM, Irwin JAG, Manners JM (1998) Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150:1459–1466

    PubMed  CAS  Google Scholar 

  • Hutchison E, Brown S, Tian C, Glass NL (2009) Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death. Microbiol SGM 155:3957–3970

    Article  CAS  Google Scholar 

  • Ishikawa FH, Souza EA, Read ND, Roa MG (2010) Live-cell imaging of conidial fusion in the bean pathogen, Colletotrichum lindemuthianum. Fungal Biol 114:2–9

    Article  PubMed  Google Scholar 

  • Liu X, Inlow M, VanEtten HD (2003) Expression profiles of pea pathogenicity (PEP) genes in vivo and in vitro, characterisation of the flanking regions of the PEP cluster and evidence that the PEP cluster region resulted from horizontal gene transfer in the fungal pathogen Nectria haematococca. Curr Genet 44:95–103

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Manners JM, Masel AM, Braithwaite KS, Irwin JAG (1992) Molecular analysis of Colletotrichum gloeosporioides pathogenic on the tropical pasture legume Stylosanthes spp. In: Bailey JA, Jeger M (eds) Colletotrichum, biology, pathology and control. CAB International, U.K., pp 250–268

    Google Scholar 

  • Manners JM, Stephenson S-A, He C, Maclean DJ (2000) Gene transfer and expression in Colletotrichum gloeosporioides causing anthracnose on Stylosanthes. In: Prusky D, Freeman S, Dickman M (eds) Host specificity, pathology and host-pathogen interactions of Colletotrichum. The American Phytopathological Society, St. Paul, pp 180–194

    Google Scholar 

  • Masel AM, Irwin JAG, Manners JM (1993) DNA addition or deletion is associated with a major karyotype polymorphism in the fungal phytopathogen Colletotrichum gloeosporioides. Mol Gen Genet 237:73–80

    Article  PubMed  CAS  Google Scholar 

  • Masel AM, He C, Poplawski AM, Irwin JAG, Manners JM (1996) Molecular evidence for chromosome transfer between biotypes of Colletotrichum gloeosporioides. Mol Plant Microb Interact 9:339–348

    Article  CAS  Google Scholar 

  • Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M’Barek S, Gohari AM, Jashni MK, Stergiopoulos I, Kema GHJ, de Wit PJGM (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev. doi:10.1111/j.1574-6976.2010.00263.x

    PubMed  Google Scholar 

  • Oliver RP, Solomon PS (2008) Recent fungal diseases of crop plants: Is lateral gene transfer a common theme? Mol Plant Microb Interact 21:287–293

    Article  CAS  Google Scholar 

  • Poplawski AM, He C, Irwin JAG, Manners JM (1997) Transfer of an autonomously replicating vector between vegetatively incompatible biotypes of Colletotrochum gloeosporioides. Curr Genet 32:66–72

    Article  PubMed  CAS  Google Scholar 

  • Rep M, Kistler HC (2010) The genomic organisation of plant pathogenicity in Fusarium species. Curr Opin Plant Biol 13:1–7

    Article  Google Scholar 

  • Ritchie BJ (2002) Mycological media and methods. In: Waller JM, Lenne JM, Waller SJ (eds) Plant pathologist’s pocket book. CAB International, U.K., pp 410–431

    Google Scholar 

  • Roca MG, Davide LC, Mendes-Costa MC, Wheals A (2003) Conidial anastomosis tubes in Colletotrichum. Fungal Genet Biol 40:138–145

    Article  PubMed  Google Scholar 

  • Roca MG, Davide LC, Davide LMC, Mendes-Costa MC, Schwan RF, Wheals AE (2004) Conidial anastomosis fusion between Colletotrichum species. Mycol Res 108:1320–1326

    Article  PubMed  Google Scholar 

  • Roca MG, Read ND, Wheals AE (2005) Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol Lett 249:191–198

    Article  CAS  Google Scholar 

  • Rodrigues-Carres MR, White G, Tsuchiya D, Taga M, VanEtten HD (2008) The supernumerary chromosome of Nectria haematococca that carries pea-pathogenicity-related genes also carries a trait for pea rhizosphere competitiveness. Appl Environ Microbiol 74:3849–3856

    Article  Google Scholar 

  • Rosewich UL, Kistler HC (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38:325–363

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Roldan MC, Kohli M, Roncero MIG, Philippsen P, Di Pietro A, Espeso EA (2010) Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum. Eukaryot Cell 9:1216–1224

    Article  PubMed  CAS  Google Scholar 

  • Stephenson S-A, Green JR, Manners JM, Maclean DJ (1997) Cloning and characterisation of glutamine synthetase from Colletotrichum gloeosporioides and demonstration of elevated expression during pathogenesis on Stylosanthes guianensis. Curr Genet 31:447–454

    Article  PubMed  CAS  Google Scholar 

  • Stephenson S-A, Hatfield J, Rusu AG, Maclean DJ, Manners JM (2000) CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol Plant Microb Interact 13:929–941

    Article  CAS  Google Scholar 

  • Temporini ED, VanEtten HD (2004) An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Nectria boniensis. Curr Genet 46:29–36

    Article  PubMed  CAS  Google Scholar 

  • Walton JD (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30:167–171

    Article  PubMed  CAS  Google Scholar 

  • Yoon C-S, Glawe DA, Shaw PD (1991) A method for rapid small-scale preparation of fungal DNA. Mycologia 83:835–838

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for the expert advice of Professor John Irwin at the University of Queensland in this study and the technical assistance of Ms Anca Rusu at CSIRO. We are grateful for funding from The Crawford Fund.

Author information

Author notes

  1. Chaozu He

    Present address: Graduate School Shenzen, Tsinghua University, The University Town, Shenzen, 518055, People’s Republic of China

Authors and Affiliations

  1. Cooperative Research Centre for Tropical Plant Pathology, University of Queensland, Brisbane, 4072, Australia

    John M. Manners & Chaozu He

  2. CSIRO Plant Industry, Queensland Bioscience Precinct, 306 Carmody Road, Brisbane, 4067, Australia

    John M. Manners

Authors
  1. John M. Manners
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chaozu He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John M. Manners.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Manners, J.M., He, C. Slow-growing heterokaryons as potential intermediates in supernumerary chromosome transfer between biotypes of Colletotrichum gloeosporioides . Mycol Progress 10, 383–388 (2011). https://doi.org/10.1007/s11557-011-0749-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-011-0749-y

Keywords

Search

Navigation