Skip to main content
SpringerLink
Log in

Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

In fungi, vegetative incompatibility is a conspecific non-self recognition mechanism that restricts formation of viable heterokaryons when incompatible alleles of specific het loci interact. In Podospora anserina, three non-allelic incompatibility systems have been genetically defined involving interactions between het-c and het-d, het-c and het-e, het-r and het-v. het-d and het-e are paralogues belonging to the HNWD gene family that encode proteins of the STAND class. HET-D and HET-E proteins comprise an N-terminal HET effector domain, a central GTP binding site and a C-terminal WD repeat domain constituted of tandem repeats of highly conserved WD40 repeat units that define the specificity of alleles during incompatibility. The WD40 repeat units of the members of this HNWD family are undergoing concerted evolution. By combining genetic analysis and gain of function experiments, we demonstrate that an additional member of this family, HNWD2, corresponds to the het-r non-allelic incompatibility gene. As for het-d and het-e, allele specificity at the het-r locus is determined by the WD repeat domain. Natural isolates show allelic variation for het-r.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Het :

Heterokaryon incompatibility gene

VI:

Vegetative incompatibility

PCD:

Programmed cell death

References

  • Belcour L, Bernet J (1969) Sur la mise en évidence d’un gène dont la mutation supprime spécifiquement certaines manifestations d’incompatibilité chez les Podospora anserina. Compte Rendu de l’Académie des Sciences de Paris. 269:712–714

    Google Scholar 

  • Bergès T, Barreau C (1989) Heat shock at an elevated temperature improves transformation efficiency of protoplasts from Podospora anserina. J Gen Microbiol 135:601–604

    PubMed  Google Scholar 

  • Bernet J (1971) Sur un cas de suppression de l’incompatibilité cellulaire chez le champignon Podospora anserina. C R Acad Sci Hebd Seances Acad Sci D 273:1120–1122

    Google Scholar 

  • Biella S, Smith ML, Aist JR, Cortesi P, Milgroom MG (2002) Programmed cell death correlates with virus transmission in a filamentous fungus. Proc Biol Sci 269:2269–2276

    Article  PubMed  Google Scholar 

  • Carroll AM, Sweigard JA, Valent B (1994) Improved vectors for selecting resistance to hygromycin. Fungal Genet Newsl 41:20–21

    Google Scholar 

  • Cortesi P, McCulloch CE, Song H, Lin H, Milgroom MG (2001) Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159:107–118

    PubMed  CAS  Google Scholar 

  • Debets F, Yang X, Griffiths AJ (1994) Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet 26:113–119

    Article  PubMed  CAS  Google Scholar 

  • Delettre YM, Bernet J (1976) Regulation of proteolytic enzymes in Podospora anserina: selection and properties of self-lysing mutant strains. Mol Gen Genet 144:191–197

    Article  PubMed  CAS  Google Scholar 

  • Dudas A, Chovanec M (2004) DNA double-strand break repair by homologous recombination. Mutat Res 566:131–167

    Article  PubMed  CAS  Google Scholar 

  • Espagne E et al. (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome biology

    Article  PubMed  Google Scholar 

  • Espagne E, Balhadere P, Begueret J, Turcq B (1997) Reactivity in vegetative incompatibility of the HET-E protein of the fungus Podospora anserina is dependent on GTP-binding activity and a WD40 repeated domain. Mol Gen Genet 256:620–627

    Article  PubMed  CAS  Google Scholar 

  • Espagne E, Balhadere P, Penin ML, Barreau C, Turcq B (2002) HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative incompatibility specificity in the fungus Podospora anserina. Genetics 161:71–81

    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 

  • Glass NL, Rasmussen C, Roca MG, Read ND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12:135–141

    Article  PubMed  CAS  Google Scholar 

  • Kaneko I, Dementhon K, Xiang Q, Glass NL (2006) Nonallelic interactions between het-c and a polymorphic locus, pin-c, are essential for nonself recognition and programmed cell death in Neurospora crassa. Genetics 172:1545–1555

    Article  PubMed  CAS  Google Scholar 

  • Koonin EV, Aravind L (2000) The NACHT family—a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci 25:223–224

    Article  PubMed  CAS  Google Scholar 

  • Labarère J (1973) Properties of an incompatibility system in Podospora anserina fungus and value of this system for the study of incompatibility. C R Acad Sci Hebd Seances Acad Sci D 276:1301–1304

    PubMed  Google Scholar 

  • Labarère J (1978) L’incompatibilité protoplasmique chez le champignon Podospora anserina: Etude génétique et biochimique, relation avec certains aspects du dévelopement et de la morphogénèse. PhD thesis

  • Labarère J, Bernet J (1977) Protoplasmic incompatibility and cell lysis in Podospora anserina. I. Genetic investigations on mutations of a novel modifier gene that suppresses cell destruction. Genetics 87:249–257

    PubMed  Google Scholar 

  • Labarère J, Begueret J, Bernet J (1974) Incompatibility in Podospora anserina: comparative properties of the antagonistic cytoplasmic factors of a nonallelic system. J Bacteriol 120:854–860

    PubMed  Google Scholar 

  • Lecellier G, Silar P (1994) Rapid methods for nucleic acids extraction from petri dish-grown mycelia. Curr Genet 25:122–123

    Article  PubMed  CAS  Google Scholar 

  • Maizels N (2005) Immunoglobulin gene diversification. Annu Rev Genet 39:23–46

    Article  PubMed  CAS  Google Scholar 

  • Milgroom MG, Cortesi P (1999) Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proc Natl Acad Sci USA 96:10518–10523

    Article  PubMed  CAS  Google Scholar 

  • Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Gaut BS (2005) Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 22:2444–2456

    Article  PubMed  CAS  Google Scholar 

  • Paoletti M, Clavé C (2007) The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryot Cell 6:2001–2008

    Article  PubMed  CAS  Google Scholar 

  • Paoletti M, Saupe SJ, Clavé C (2007) Genesis of a fungal non self recognition repertoire. PLoS ONE 2:e283

    Article  PubMed  Google Scholar 

  • Pinan-Lucarré B, Paoletti M, Clavé C (2007) Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17:101–111

    Article  PubMed  Google Scholar 

  • Saupe SJ (2000) Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64:489–502

    Article  PubMed  CAS  Google Scholar 

  • Saupe S, Descamps C, Turcq B, Begueret J (1994) Inactivation of the Podospora anserina vegetative incompatibility locus het-c, whose product resembles a glycolipid transfer protein, drastically impairs ascospore production. Proc Natl Acad Sci USA 91:5927–5931

    Article  PubMed  CAS  Google Scholar 

  • Saupe S, Turcq B, Begueret J (1995a) A gene responsible for vegetative incompatibility in the fungus Podospora anserina encodes a protein with a GTP-binding motif and G beta homologous domain. Gene 162:135–139

    Article  PubMed  CAS  Google Scholar 

  • Saupe S, Turcq B, Begueret J (1995b) Sequence diversity and unusual variability at the het-c locus involved in vegetative incompatibility in the fungus Podospora anserina. Curr Genet 27:466–471

    Article  PubMed  CAS  Google Scholar 

  • Saupe SJ, Kuldau GA, Smith ML, Glass NL (1996) The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics 143:1589–1600

    PubMed  CAS  Google Scholar 

  • Saupe SJ, Clavé C, Begueret J (2000) Vegetative incompatibility in filamentous fungi: Podospora and Neurospora provide some clues. Curr Opin Microbiol 3:608–612

    Article  PubMed  CAS  Google Scholar 

  • Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395

    Article  PubMed  CAS  Google Scholar 

  • Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185

    Article  PubMed  CAS  Google Scholar 

  • Smith ML, Micali OC, Hubbard SP, Mir-Rashed N, Jacobson DJ, Glass NL (2000) Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 155:1095–1104

    PubMed  CAS  Google Scholar 

  • Tock MR, Dryden DT (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472

    Article  PubMed  CAS  Google Scholar 

  • van der Gaag M, Debets AJ, Oosterhof J, Slakhorst M, Thijssen JA, Hoekstra RF (2000) Spore-killing meiotic drive factors in a natural population of the fungus Podospora anserina. Genetics 156:593–605

    PubMed  Google Scholar 

  • van Diepeningen AD, Debets AJ, Slakhorst SM, Hoekstra RF (2008) Mitochondrial pAL2–1 plasmid homologs are senescence factors in Podospora anserina independent of intrinsic senescence. Biotechnol J 3:791–802

    Article  PubMed  Google Scholar 

  • Wu J, Saupe SJ, Glass NL (1998) Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci USA 95:12398–12403

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Dr. F. Ness for critical reading of the manuscript, Mme M. Sicault for invaluable technical assistance, and the EU (Transdeath grant # 511983), the Agence Nationale pour la Recherche (ANR SexDevMyco # NT-1_41707) and the Conseil Régional d’Aquitaine (#2005130009AB) for funding.

Author information

Authors and Affiliations

  1. Laboratoire de Génétique Moléculaire des Champignons, IBGC, UMR5095, Université Victor Segalen Bordeaux2 et CNRS, 1 rue Camille Saint-Saëns, 33077, Bordeaux Cedex, France

    Damien Chevanne, Sven J. Saupe, Corinne Clavé & Mathieu Paoletti

  2. Laboratory of Genetics, Wageningen University, Arboretumlaan 4, 6703 BD, Wageningen, The Netherlands

    Eric Bastiaans & Alfons Debets

Authors
  1. Damien Chevanne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric Bastiaans
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alfons Debets
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sven J. Saupe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Corinne Clavé
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mathieu Paoletti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mathieu Paoletti.

Additional information

Communicated by U. Kueck.

Sequence data reported here are available in the Genbank database under accession numbers FJ269240 and FJ269239 for het-r and het-R, respectively.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chevanne, D., Bastiaans, E., Debets, A. et al. Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family. Curr Genet 55, 93–102 (2009). https://doi.org/10.1007/s00294-008-0227-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-008-0227-5

Keywords

Search

Navigation