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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
Anagnostakis S. L. and Waggoner P. E. 1981 Hypovirulence, vegetative incompatibility, and the growth of cankers of chestnut blight.Phytopathology 71: 1198–1202
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
Beadle G. W. and Coonradt V. L. 1944 Heterocaryosis inNeurospora crassa.Genetics 29: 291–307
Bégueret J. 1972 Protoplasmic incompatibility: Possible involvement of proteolytic enzymes.Nature New Biol. 235: 56–58
Begueret J. and Bernet J. 1973 Proteolytic enzymes and protoplasmic incompatibility in the fungusPodospora anserina.Nature New Biol. 243: 94–96
Begueret J., Turcq B. and Clavé C. 1994 Vegetative incompatibility in filamentous fungi:het genes begin to talk.Trends Genet. 10: 441–446
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
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
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
Caten C. E. 1972 Vegetative incompatibility and cytoplasmic infection in fungi.J. Gen. Microbiol. 72: 221–229
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
Correll J. G, Klittich C. J. R. and Leslie J. F. 1989 Heterokaryon self-incompatibility inGibberella fujikuroi (Fusarium moniliforme).Mycol. Res. 93: 21–27
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
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
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
Durrens P. and Bernet J. 1982Podospora anserina mutations inhibiting several developmental alternatives and growth renewal.curr. Genet. 5: 181–185
Ferenczy L., Szegedi M. and Kevei F. 1977 Interspecific protoplast fusion and complementation inAspergilli.Experiential 33: 184–186
Garnjobst L. 1953 Genetic control of heterocaryosis inNeurospora crassa.Am. J. Bot. 40: 607–614
Garnjobst L. 1955 Further analysis of genetic control of heterocaryosis inNeurospora crassa.Am. J. Bot. 42: 444–448
Garnjobst L. and Wilson J. F. 1956 Heterokaryosis and protoplasmic incompatibility inNeurospora crassa.Proc. Natl. Acad. Sci. USA 42: 613–618
Glass N. L. and Kuldau G. A. 1992 Mating type and vegetative incompatibility in filamentous ascomycetes.Annu. Rev. Phytopathol. 30: 201–224
Glass N. L., Grotelueschen J. and Metzenberg R. L. 1990Neurospora crassa A mating-type region.Proc. Natl. Acad. Sci. USA 87: 4912–4916
Griffiths A. J. F. 1982 Null mutants of theA anda mating type alleles ofNeurospora crassa.Can. J. Genet. Cytol. 24: 167–176
Griffiths A, J. F. and Delange A. M. 1978 Mutations of thea mating type gene inNeurospora crassa.Genetics 88: 239–254
Hartl D. L, Dempster E. R. and Brown S. W. 1975 Adaptive significance of vegetative incompatibility inNeurospora crassa.Genetics 81: 553–569
Herskowitz I. 1995 MAP kinase pathways in yeast: for mating and more.Cell 80: 187–197
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
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
Jacobson D. J. 1992 Control of mating type heterokaryon incompatibility by thetol gene inNeurospora crassa andN.tetrasperma. Genome 35: 347–353
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
Johnson T. E. 1979 ANeurospora mutation that arrests perithecial development as either male or female parent.Genetics 92: 1107–1120
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
Labarere J. and Bernet J. 1979a A pleiotropic mutation affecting protoperithecium formation and ascospore growth. J.Gen. Microbiol. 113: 19–27
Labarere J. and Bernet J. 1979b Protoplasmic incompatibility inPodospora anserina: A possible role for its associated proteolytic activity.Genetics 93: 525–537
Leslie J. F. 1993 Fungal vegetative compatibility.Annu. Rev. Phytopathol. 31: 127–150
Leslie J. F. 1996 Fungal vegetative compatibility—promises and prospects.Phytoparasitica 24; 3–6
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
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
Molnar A., Sulyok L. and Hornok L. 1990 Parasexual recombination between vegetatively incompatible strains inFusarium oxysporum.Mycol. Res. 94: 393–398
Mylyk O. M. 1975 Heterokaryon incompatibility genes inNewospora crassa detected using duplicationproducing chromosome rearrangements.Genetics 80: 107–124
Mylyk O. M. 1976 Heteromorphism for heterokaryon incompatibility genes in natural populations ofNeicrospora crassa.Genetics 83: 275–284
Newmeyer D. 1970 A suppressor of the heterokaryon-incompatibility associated with mating type inNewospora crassa.Can. J. Genet. Cytol. 12: 914–926
Newmeyer D. and Taylor C. W. 1967 A pericentric inversion inNewospora, with unstable duplication progeny.Genetics 56: 771–791
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
Peberdy J. F. and Ferenczy L., eds. 1985Fungal protoplasts: applications in biochemistry and genetics (New York: Marcel Dekker)
Perkins D. D. 1975 The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes inNewospora.Genetics 80: 87–105
Philley M. L. and Staben C. 1994 Functional analyses of theNewospora crassa MT a-1 mating type polypeptide.Genetics 137: 715–722
Pittenger T. H. and Brawner T. G. 1961 Genetic control of nuclear selection inNewospora heterokaryons.Genetics 46: 1645–1663
Rayner A. D. M. 1991 The phytopathological significance of mycelial individualism.Annu. Rev. Phytopathol. 29: 305–323
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
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 andGβ homologous domain.Gene 162: 135–139
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
Staben C. and Yanofsky C. 1990Newospora crassa a mating type region.Proc. Natl. Acad. Sci. USA 87: 4917–4921
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
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
Vaux D. L. and Strasser A. 1996 The molecular biology of apoptosis.Proc. Natl. Acad. Sci. USA 93: 2239–2244
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
Williams C. A. and Wilson J. F. 1966 Cytoplasmic incompatibility reactions inNewospora crassa.Ann. New York Acad. Sci. 129: 853–863
Williams G. T. and Smith C. A. 1993 Molecular recognition of apoptosis: Genetic controls on cell death.Cell 74: 777–779
Wilson J. F and Garnjobst L. 1966 A new incompatibility locus inNeuwspora crassa.Genetics 53: 621–631
Wilson J. F., Garnjobst L. and Tatum E. L. 1961 Heterocaryon incompatibility inNewospora crassa— microinjection studies.Am. J. Bot. 48: 299–305
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
Zeller K. A. and Leslie J. F. 1996 Some mutants that overcome vegetative incompatibility inFusarium moniliforme (Gibberella fujikuroi mating population A).Phytopathology 86: S32
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Issue Date:
DOI: https://doi.org/10.1007/BF02966319