Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Jun;161(2):633–641. doi: 10.1093/genetics/161.2.633

Multilocus self-recognition systems in fungi as a cause of trans-species polymorphism.

Christina A Muirhead 1, N Louise Glass 1, Montgomery Slatkin 1
PMCID: PMC1462126  PMID: 12072460

Abstract

Trans-species polymorphism, meaning the presence of alleles in different species that are more similar to each other than they are to alleles in the same species, has been found at loci associated with vegetative incompatibility in filamentous fungi. If individuals differ at one or more of these loci (termed het for heterokaryon), they cannot form stable heterokaryons after vegetative fusion. At the het-c locus in Neurospora crassa and related species there is clear evidence of trans-species polymorphism: three alleles have persisted for approximately 30 million years. We analyze a population genetic model of multilocus vegetative incompatibility and find the conditions under which trans-species polymorphism will occur. In the model, several unlinked loci determine the vegetative compatibility group (VCG) of an individual. Individuals of different VCGs fail to form productive heterokaryons, while those of the same VCG form viable heterokaryons. However, viable heterokaryon formation between individuals of the same VCG results in a loss in fitness, presumably via transfer of infectious agents by hyphal fusion or exploitation by aggressive genotypes. The result is a form of balancing selection on all loci affecting an individual's VCG. We analyze this model by making use of a Markov chain/strong selection, weak mutation (SSWM) approximation. We find that trans-species polymorphism of the type that has been found at the het-c locus is expected to occur only when the appearance of new incompatibility alleles is strongly constrained, because the rate of mutation to such alleles is very low, because the number of possible incompatibility alleles at each locus is restricted, or because the number of incompatibility loci is limited.

Full Text

The Full Text of this article is available as a PDF (113.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anwar M. M., Croft J. H., Dales R. B. Analysis of heterokaryon incompatibility between heterokaryon-compatibility (h-c) groups R and GL provides evidence that at least eight het loci control somatic incompatibility in Aspergillus nidulans. J Gen Microbiol. 1993 Jul;139(7):1599–1603. doi: 10.1099/00221287-139-7-1599. [DOI] [PubMed] [Google Scholar]
  2. Arden B., Klein J. Biochemical comparison of major histocompatibility complex molecules from different subspecies of Mus musculus: evidence for trans-specific evolution of alleles. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2342–2346. doi: 10.1073/pnas.79.7.2342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bjorkman P. J., Parham P. Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem. 1990;59:253–288. doi: 10.1146/annurev.bi.59.070190.001345. [DOI] [PubMed] [Google Scholar]
  4. Bégueret J., Turcq B., Clavé C. Vegetative incompatibility in filamentous fungi: het genes begin to talk. Trends Genet. 1994 Dec;10(12):441–446. doi: 10.1016/0168-9525(94)90115-5. [DOI] [PubMed] [Google Scholar]
  5. Clarke A. E., Newbigin E. Molecular aspects of self-incompatibility in flowering plants. Annu Rev Genet. 1993;27:257–279. doi: 10.1146/annurev.ge.27.120193.001353. [DOI] [PubMed] [Google Scholar]
  6. Cortesi P, Milgroom MG. Genetics of vegetative incompatibility in cryphonectria parasitica . Appl Environ Microbiol. 1998 Aug;64(8):2988–2994. doi: 10.1128/aem.64.8.2988-2994.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Debets F., Yang X., Griffiths A. J. Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet. 1994 Aug;26(2):113–119. doi: 10.1007/BF00313797. [DOI] [PubMed] [Google Scholar]
  8. Figueroa F., Günther E., Klein J. MHC polymorphism pre-dating speciation. Nature. 1988 Sep 15;335(6187):265–267. doi: 10.1038/335265a0. [DOI] [PubMed] [Google Scholar]
  9. Glass N. L., Jacobson D. J., Shiu P. K. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet. 2000;34:165–186. doi: 10.1146/annurev.genet.34.1.165. [DOI] [PubMed] [Google Scholar]
  10. Hartl D. L., Dempster E. R., Brown S. W. Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics. 1975 Nov;81(3):553–569. doi: 10.1093/genetics/81.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ioerger T. R., Clark A. G., Kao T. H. Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9732–9735. doi: 10.1073/pnas.87.24.9732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jinks J. L., Caten C. E., Simchen G., Croft J. H. Heterokaryon incompatibility and variation in wild populations of Aspergillus nidulans. Heredity (Edinb) 1966 May;21(2):227–239. doi: 10.1038/hdy.1966.20. [DOI] [PubMed] [Google Scholar]
  13. Kelly J. K., Wade M. J. Molecular evolution near a two-locus balanced polymorphism. J Theor Biol. 2000 May 7;204(1):83–101. doi: 10.1006/jtbi.2000.2003. [DOI] [PubMed] [Google Scholar]
  14. Leslie J. F. Fungal vegetative compatibility. Annu Rev Phytopathol. 1993;31:127–150. doi: 10.1146/annurev.py.31.090193.001015. [DOI] [PubMed] [Google Scholar]
  15. Milgroom M. G., Cortesi P. Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10518–10523. doi: 10.1073/pnas.96.18.10518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mir-Rashed N., Jacobson D. J., Dehghany M. R., Micali O. C., Smith M. L. Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol. 2000 Aug;30(3):197–205. doi: 10.1006/fgbi.2000.1218. [DOI] [PubMed] [Google Scholar]
  17. Mylyk O. M. Heteromorphism for Heterokaryon Incompatibility Genes in Natural Populations of NEUROSPORA CRASSA. Genetics. 1976 Jun;83(2):275–284. doi: 10.1093/genetics/83.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. PONTECORVO G. The parasexual cycle in fungi. Annu Rev Microbiol. 1956;10:393–400. doi: 10.1146/annurev.mi.10.100156.002141. [DOI] [PubMed] [Google Scholar]
  19. Pandit A, Maheshwari R. A Demonstration of the Role of het Genes in Heterokaryon Formation in Neurospora under Simulated Field Conditions. Fungal Genet Biol. 1996 Mar;20(1):99–102. doi: 10.1006/fgbi.1996.0017. [DOI] [PubMed] [Google Scholar]
  20. Perkins D. D., Davis R. H. Neurospora at the millennium. Fungal Genet Biol. 2000 Dec;31(3):153–167. doi: 10.1006/fgbi.2000.1248. [DOI] [PubMed] [Google Scholar]
  21. Powell A. J., Jacobson D. J., Natvig D. O. Allelic diversity at the het-c locus in Neurospora tetrasperma confirms outcrossing in nature and reveals an evolutionary dilemma for pseudohomothallic ascomycetes. J Mol Evol. 2001 Jan;52(1):94–102. doi: 10.1007/s002390010138. [DOI] [PubMed] [Google Scholar]
  22. Saupe S. J., Clavé C., Bégueret J. Vegetative incompatibility in filamentous fungi: Podospora and Neurospora provide some clues. Curr Opin Microbiol. 2000 Dec;3(6):608–612. doi: 10.1016/s1369-5274(00)00148-x. [DOI] [PubMed] [Google Scholar]
  23. Saupe S. J., Glass N. L. Allelic specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa is determined by a highly variable domain. Genetics. 1997 Aug;146(4):1299–1309. doi: 10.1093/genetics/146.4.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saupe S. J. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev. 2000 Sep;64(3):489–502. doi: 10.1128/mmbr.64.3.489-502.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Skupski MP, Jackson DA, Natvig DO. Phylogenetic Analysis of Heterothallic Neurospora Species. Fungal Genet Biol. 1997 Feb;21(1):153–162. [PubMed] [Google Scholar]
  26. Slatkin M. Balancing selection at closely linked, overdominant loci in a finite population. Genetics. 2000 Mar;154(3):1367–1378. doi: 10.1093/genetics/154.3.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Slatkin M., Muirhead C. A. Overdominant alleles in a population of variable size. Genetics. 1999 Jun;152(2):775–781. doi: 10.1093/genetics/152.2.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Takahata N. A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2419–2423. doi: 10.1073/pnas.87.7.2419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vekemans X., Slatkin M. Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics. 1994 Aug;137(4):1157–1165. doi: 10.1093/genetics/137.4.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wright S. The Distribution of Self-Sterility Alleles in Populations. Genetics. 1939 Jun;24(4):538–552. doi: 10.1093/genetics/24.4.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wu J., Saupe S. J., Glass N. L. Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12398–12403. doi: 10.1073/pnas.95.21.12398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. van Diepeningen A. D., Debets A. J., Hoekstra R. F. Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet. 1997 Sep;32(3):209–217. doi: 10.1007/s002940050268. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES