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Heterokaryon incompatibility in fungi—more than just another way to die

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Abstract

In filamentous fungi heterokaryon (vegetative) compatibility is regulated by a number of different loci. Vegetative incompatibility is most often detected as the inability to form a prototrophic heterokaryon under forcing conditions, or as the formation of a barrage when two incompatible strains interact. Vegetative compatibility has been used as a multilocus phenotype in analysis of fungal populations. In some highly clonal populations the vegetative-compatibility phenotype is correlated with pathogenicity. The molecular basis for vegetative compatibility is not well understood. Fourhet loci have been cloned fromNeurospora crasset orPodospora anserina, inch but no two are alike and it is clear that thehet genes themselves do not encode the gene products that are directly responsible for cell death. We suggest that a broader view of vegetative compatibility would include genes that are responsible for prefusion, fusion, and postfusion activities. Postfusion activities could include the fungal apoptotic apparatus since microscopic observations of cell death resemble those in higher plants and animals.

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References

  • Adams G., Johnson N., Leslie J. and Hart L. P. 1987 Heterokaryons ofGibberella zeae formed following hyphal anastomosis or protoplast fusion.Exp. Mycol. 11: 339–353

    Article  Google Scholar 

  • Anagnostakis S. L. and Waggoner P. E. 1981 Hypovirulence, vegetative incompatibility, and the growth of cankers of chestnut blight.Phytopathology 71: 1198–1202

    Article  Google Scholar 

  • Arganoza M. T., Ohraberger J., Min J. and Akins R. A. 1994 Suppressor mutants ofNeurospora crassa that tolerate allelic differences at single or multiple heterokaryon incompatibility loci.Genetics 137: 731–742

    PubMed  CAS  Google Scholar 

  • Beadle G. W. and Coonradt V. L. 1944 Heterocaryosis inNeurospora crassa.Genetics 29: 291–307

    PubMed  CAS  Google Scholar 

  • Bégueret J. 1972 Protoplasmic incompatibility: Possible involvement of proteolytic enzymes.Nature New Biol. 235: 56–58

    PubMed  Google Scholar 

  • Begueret J. and Bernet J. 1973 Proteolytic enzymes and protoplasmic incompatibility in the fungusPodospora anserina.Nature New Biol. 243: 94–96

    Article  PubMed  CAS  Google Scholar 

  • Begueret J., Turcq B. and Clavé C. 1994 Vegetative incompatibility in filamentous fungi:het genes begin to talk.Trends Genet. 10: 441–446

    Article  PubMed  CAS  Google Scholar 

  • Bernet J. 1992 A gene suppressing the allelic protoplasmic incompatibility specified by genes at five different loci inPodospora anserina.J. Gen. Microbiol. 138: 2567–2574

    CAS  Google Scholar 

  • Boucherie H. and Bernet J. 1974 Protoplasmic incompatibility and female organ formation inPodospora anserina: Properties of mutations abolishing both processes.Mol. Gen. Genet. 135: 163–174

    Article  PubMed  CAS  Google Scholar 

  • Bourges N., Paoletti M., Clave C. and Bégueret J. 1996 Vegetative incompatibility inPodospora anserina: Identification of proteins involved in cell death.Fungal Genet. Newsl. 43B: 9

    Google Scholar 

  • Caten C. E. 1972 Vegetative incompatibility and cytoplasmic infection in fungi.J. Gen. Microbiol. 72: 221–229

    PubMed  CAS  Google Scholar 

  • Correll J. C, Klittich C. J. R. and Leslie J. F. 1987 Nitrate nonutilizing mutants ofFusarium oxysporum and their use in vegetative compatibility tests.Phytopathology 77: 1640–1646

    Article  Google Scholar 

  • Correll J. G, Klittich C. J. R. and Leslie J. F. 1989 Heterokaryon self-incompatibility inGibberella fujikuroi (Fusarium moniliforme).Mycol. Res. 93: 21–27

    Article  Google Scholar 

  • Dales R. B. G. and Croft J. H. 1977 Protoplast fusion and the isolation of heterokaryons and diploids from vegetatively compatible strains ofAspergillus nidulans.FEMS Microbiol. Lett. 1: 201–204

    Article  Google Scholar 

  • Delettre Y. M., Boucherie H. and Bernet J. 1978 Protoplasmic incompatibility and cell lysis inPodospora anserina: effect of b-phenyl pyruvic acid.Biochem. Physiol. Pflanz. 172: 27–34

    CAS  Google Scholar 

  • Deleu C, Clavé C. and Bégueret J. 1993 A single amino acid difference is sufficient to elicit vegetative incompatibility in the fungusPodospora anserina.Genetics 135: 45–52

    PubMed  CAS  Google Scholar 

  • Durrens P. and Bernet J. 1982Podospora anserina mutations inhibiting several developmental alternatives and growth renewal.curr. Genet. 5: 181–185

    Article  Google Scholar 

  • Ferenczy L., Szegedi M. and Kevei F. 1977 Interspecific protoplast fusion and complementation inAspergilli.Experiential 33: 184–186

    Article  CAS  Google Scholar 

  • Garnjobst L. 1953 Genetic control of heterocaryosis inNeurospora crassa.Am. J. Bot. 40: 607–614

    Article  Google Scholar 

  • Garnjobst L. 1955 Further analysis of genetic control of heterocaryosis inNeurospora crassa.Am. J. Bot. 42: 444–448

    Article  Google Scholar 

  • Garnjobst L. and Wilson J. F. 1956 Heterokaryosis and protoplasmic incompatibility inNeurospora crassa.Proc. Natl. Acad. Sci. USA 42: 613–618

    Article  PubMed  CAS  Google Scholar 

  • Glass N. L. and Kuldau G. A. 1992 Mating type and vegetative incompatibility in filamentous ascomycetes.Annu. Rev. Phytopathol. 30: 201–224

    Article  PubMed  CAS  Google Scholar 

  • Glass N. L., Grotelueschen J. and Metzenberg R. L. 1990Neurospora crassa A mating-type region.Proc. Natl. Acad. Sci. USA 87: 4912–4916

    Article  PubMed  CAS  Google Scholar 

  • Griffiths A. J. F. 1982 Null mutants of theA anda mating type alleles ofNeurospora crassa.Can. J. Genet. Cytol. 24: 167–176

    Google Scholar 

  • Griffiths A, J. F. and Delange A. M. 1978 Mutations of thea mating type gene inNeurospora crassa.Genetics 88: 239–254

    PubMed  Google Scholar 

  • Hartl D. L, Dempster E. R. and Brown S. W. 1975 Adaptive significance of vegetative incompatibility inNeurospora crassa.Genetics 81: 553–569

    PubMed  CAS  Google Scholar 

  • Herskowitz I. 1995 MAP kinase pathways in yeast: for mating and more.Cell 80: 187–197

    Article  PubMed  CAS  Google Scholar 

  • Howlett B. J., Leslie J. F. and Perkins D. D. 1993 Putative multiple alleles at the vegetative (heterokaryon) incompatibility locihet-c andhet-8 inNeurospora crassa.Fungal Genet. Newsl. 40: 40–42

    Google Scholar 

  • Hyakumachi M. and Ui T. 1987 Non-self-anastomosing isolates ofRhizoctoniasolani obtained from fields of sugar beet monoculture.Trans. Br. Mycol. Soc. 89: 155–159

    Article  Google Scholar 

  • Jacobson D. J. 1992 Control of mating type heterokaryon incompatibility by thetol gene inNeurospora crassa andN.tetrasperma. Genome 35: 347–353

    CAS  Google Scholar 

  • Jacobson D. J., Ohrnberger J. and Akins R. A. 1995 The Wilson-Garnjobstheterokaryon-incompatibility tester strains ofNeurospora crassa contain modifiers which inluence growth rate of heterokaryons and distort segregation ratios.Fungal Genet. Newsl. 42: 34–40

    Google Scholar 

  • Johnson T. E. 1979 ANeurospora mutation that arrests perithecial development as either male or female parent.Genetics 92: 1107–1120

    PubMed  Google Scholar 

  • Kuhn D. N., Cortes B., Pinto T., Recalde G. and D’Alessio N. 1996 Inter-vegetative compatibility group, inter-forma species, and inter-species heterokaryon formation inFusarium.Phytopathology 86: S32–33

    Google Scholar 

  • Labarere J. and Bernet J. 1979a A pleiotropic mutation affecting protoperithecium formation and ascospore growth. J.Gen. Microbiol. 113: 19–27

    CAS  Google Scholar 

  • Labarere J. and Bernet J. 1979b Protoplasmic incompatibility inPodospora anserina: A possible role for its associated proteolytic activity.Genetics 93: 525–537

    PubMed  CAS  Google Scholar 

  • Leslie J. F. 1993 Fungal vegetative compatibility.Annu. Rev. Phytopathol. 31: 127–150

    Article  PubMed  CAS  Google Scholar 

  • Leslie J. F. 1996 Fungal vegetative compatibility—promises and prospects.Phytoparasitica 24; 3–6

    Google Scholar 

  • Leslie J. F. and Klein K. K. 1996 Female fertility and mating type effects on effective population size and evolution in filamentous fungi.Genetics 144: 557–567

    PubMed  CAS  Google Scholar 

  • Leslie J. F. and Yamashiro C. T. 1997 Effects of thetol mutation on allelic interactions athet loci inNeurospora crassa. Genome (submitted)

  • Milgroom M. G. 1996 Recombination and the multi-locus structure of fungal populations.Annu. Rev. Phytopathol. 34: 457–477

    Article  PubMed  CAS  Google Scholar 

  • Molnar A., Sulyok L. and Hornok L. 1990 Parasexual recombination between vegetatively incompatible strains inFusarium oxysporum.Mycol. Res. 94: 393–398

    Google Scholar 

  • Mylyk O. M. 1975 Heterokaryon incompatibility genes inNewospora crassa detected using duplicationproducing chromosome rearrangements.Genetics 80: 107–124

    PubMed  CAS  Google Scholar 

  • Mylyk O. M. 1976 Heteromorphism for heterokaryon incompatibility genes in natural populations ofNeicrospora crassa.Genetics 83: 275–284

    PubMed  Google Scholar 

  • Newmeyer D. 1970 A suppressor of the heterokaryon-incompatibility associated with mating type inNewospora crassa.Can. J. Genet. Cytol. 12: 914–926

    PubMed  CAS  Google Scholar 

  • Newmeyer D. and Taylor C. W. 1967 A pericentric inversion inNewospora, with unstable duplication progeny.Genetics 56: 771–791

    PubMed  CAS  Google Scholar 

  • Newmeyer D., Howe H. B. Jr and Galeazzi D. R. 1973 A search for complexity at the mating-type locus ofNewospora crassa.Can. J. Genet. Cytol 15: 577–585

    PubMed  CAS  Google Scholar 

  • Peberdy J. F. and Ferenczy L., eds. 1985Fungal protoplasts: applications in biochemistry and genetics (New York: Marcel Dekker)

    Google Scholar 

  • Perkins D. D. 1975 The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes inNewospora.Genetics 80: 87–105

    PubMed  CAS  Google Scholar 

  • Philley M. L. and Staben C. 1994 Functional analyses of theNewospora crassa MT a-1 mating type polypeptide.Genetics 137: 715–722

    PubMed  CAS  Google Scholar 

  • Pittenger T. H. and Brawner T. G. 1961 Genetic control of nuclear selection inNewospora heterokaryons.Genetics 46: 1645–1663

    PubMed  CAS  Google Scholar 

  • Rayner A. D. M. 1991 The phytopathological significance of mycelial individualism.Annu. Rev. Phytopathol. 29: 305–323

    Article  Google Scholar 

  • Saupe S., Descamps C, Turcq B. and Begueret J. 1994 Inactivation of thePodospora anserina vegetative incompatibility locushet-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. and Begueret J. 1995 A gene responsible for vegetative incompatibility in the fungusPodospora anserina encodes a protein with a GTP-binding motif and homologous domain.Gene 162: 135–139

    Article  PubMed  CAS  Google Scholar 

  • Saupe S. J., Kuldau G. A., Smith M. L. and Glass N. L. 1996 The product of thehet-C heterokaryon compatibility gene ofNewospora crassa has characteristics of a glycine-rich cell wall protein.Genetics 143: 1589–1600

    PubMed  CAS  Google Scholar 

  • Staben C. and Yanofsky C. 1990Newospora crassa a mating type region.Proc. Natl. Acad. Sci. USA 87: 4917–4921

    Article  PubMed  CAS  Google Scholar 

  • Stasz T. E., Harman G. E. and Gullino M. L. 1989 Limited vegetative compatibility following intra- and interspecific protoplast fusion inTrichoderma.Exp. Mycol. 13: 364–371

    Article  Google Scholar 

  • Turcq B., Denayrolles M.and Bégueret J. 1990 Isolation of the two allelic incompatibility geness andS of the fungusPodospora anserina.Curr. Genet. 17: 297–303

    Article  CAS  Google Scholar 

  • Vaux D. L. and Strasser A. 1996 The molecular biology of apoptosis.Proc. Natl. Acad. Sci. USA 93: 2239–2244

    Article  PubMed  CAS  Google Scholar 

  • Wang H., Li J., Bostock R. M. and Gilchrist D. G. 1996 Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development.Plant Cell 8: 375–391

    Article  PubMed  CAS  Google Scholar 

  • Williams C. A. and Wilson J. F. 1966 Cytoplasmic incompatibility reactions inNewospora crassa.Ann. New York Acad. Sci. 129: 853–863

    Article  CAS  Google Scholar 

  • Williams G. T. and Smith C. A. 1993 Molecular recognition of apoptosis: Genetic controls on cell death.Cell 74: 777–779

    Article  PubMed  CAS  Google Scholar 

  • Wilson J. F and Garnjobst L. 1966 A new incompatibility locus inNeuwspora crassa.Genetics 53: 621–631

    PubMed  CAS  Google Scholar 

  • Wilson J. F., Garnjobst L. and Tatum E. L. 1961 Heterocaryon incompatibility inNewospora crassa— microinjection studies.Am. J. Bot. 48: 299–305

    Article  Google Scholar 

  • Woudt L. P., Neuvell A., Sikkema A., de Milliano W. A. J., Campbell C. L. and Leslie J. F. 1995Fusarium from cyclamens.Phytopathology 85: 1348–1355

    Article  Google Scholar 

  • Zeller K. A. and Leslie J. F. 1996 Some mutants that overcome vegetative incompatibility inFusarium moniliforme (Gibberella fujikuroi mating population A).Phytopathology 86: S32

    Google Scholar 

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Leslie, J.F., Zeller, K.A. Heterokaryon incompatibility in fungi—more than just another way to die. J. Genet. 75, 415–424 (1996). https://doi.org/10.1007/BF02966319

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