Skip to main content
Genetics logoLink to Genetics
. 1998 Jun;149(2):915–926. doi: 10.1093/genetics/149.2.915

The mod-A suppressor of nonallelic heterokaryon incompatibility in Podospora anserina encodes a proline-rich polypeptide involved in female organ formation.

C Barreau 1, M Iskandar 1, G Loubradou 1, V Levallois 1, J Bégueret 1
PMCID: PMC1460161  PMID: 9611202

Abstract

Vegetative incompatibility in fungi results from the control of heterokaryon formation by the genes present at het loci. Coexpression of antagonistic het genes in the same hyphae leads to a lethal process. In Podospora anserina, self-incompatible strains containing nonallelic incompatible genes in the same nucleus are inviable as the result of a growth arrest and a lytic process. Mutations in suppressor genes (mod genes) can restore the viability. These mod mutations also interfere with developmental processes, which suggests common steps between the incompatibility reaction and cellular differentiation. The mod-A locus, responsible for growth arrest in the self-incompatible strains, is also involved in the control of the development of female organs. The mod-A gene was isolated. An open reading frame 687 amino acids long was identified. The MOD-A-encoded polypeptide is rich in proline residues, which are clustered in a domain containing a motif that displays similarity to SH3-binding motifs, which are known to be involved in protein-protein interactions. Construction of a strain deleted for mod-A confirmed that the product of this gene involved in differentiation is a key regulator of growth arrest associated with vegetative incompatibility.

Full Text

The Full Text of this article is available as a PDF (381.8 KB).

Selected References

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

  1. Altschul S. F., Boguski M. S., Gish W., Wootton J. C. Issues in searching molecular sequence databases. Nat Genet. 1994 Feb;6(2):119–129. doi: 10.1038/ng0294-119. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Arganoza M. T., Ohrnberger J., Min J., Akins R. A. Suppressor mutants of Neurospora crassa that tolerate allelic differences at single or at multiple heterokaryon incompatibility loci. Genetics. 1994 Jul;137(3):731–742. doi: 10.1093/genetics/137.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ballance D. J. Sequences important for gene expression in filamentous fungi. Yeast. 1986 Dec;2(4):229–236. doi: 10.1002/yea.320020404. [DOI] [PubMed] [Google Scholar]
  5. Bergès T., Barreau C. Heat shock at an elevated temperature improves transformation efficiency of protoplasts from Podospora anserina. J Gen Microbiol. 1989 Mar;135(3):601–604. doi: 10.1099/00221287-135-3-601. [DOI] [PubMed] [Google Scholar]
  6. Bernet J., Bégueret J., Labarére J. Incompatibility in the fungus Podospora anserina. Are the mutations abolishing the incompatibility reaction ribosomal mutations? Mol Gen Genet. 1973 Jul 31;124(1):35–50. doi: 10.1007/BF00267162. [DOI] [PubMed] [Google Scholar]
  7. Boucherie H., Bernet J. Protoplasmic Incompatibility in PODOSPORA ANSERINA: a Possible Function for Incompatibility Genes. Genetics. 1980 Oct;96(2):399–411. doi: 10.1093/genetics/96.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boucherie H., Bernet J. Protoplasmic incompatibility and female organ formation in Podospora anserina: Properties of mutations abolishing both processes. Mol Gen Genet. 1974;135(2):163–174. doi: 10.1007/BF00264783. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Chenevert J., Corrado K., Bender A., Pringle J., Herskowitz I. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature. 1992 Mar 5;356(6364):77–79. doi: 10.1038/356077a0. [DOI] [PubMed] [Google Scholar]
  11. Cohen G. B., Ren R., Baltimore D. Modular binding domains in signal transduction proteins. Cell. 1995 Jan 27;80(2):237–248. doi: 10.1016/0092-8674(95)90406-9. [DOI] [PubMed] [Google Scholar]
  12. Donnelly S. F., Pocklington M. J., Pallotta D., Orr E. A proline-rich protein, verprolin, involved in cytoskeletal organization and cellular growth in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1993 Nov;10(3):585–596. doi: 10.1111/j.1365-2958.1993.tb00930.x. [DOI] [PubMed] [Google Scholar]
  13. Espagne E., Balhadère P., Bégueret J., Turcq B. 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. 1997 Nov;256(6):620–627. doi: 10.1007/s004380050610. [DOI] [PubMed] [Google Scholar]
  14. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Giasson L., Kronstad J. W. Mutations in the myp1 gene of Ustilago maydis attenuate mycelial growth and virulence. Genetics. 1995 Oct;141(2):491–501. doi: 10.1093/genetics/141.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Glass N. L., Grotelueschen J., Metzenberg R. L. Neurospora crassa A mating-type region. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4912–4916. doi: 10.1073/pnas.87.13.4912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Glass N. L., Kuldau G. A. Mating type and vegetative incompatibility in filamentous ascomycetes. Annu Rev Phytopathol. 1992;30:201–224. doi: 10.1146/annurev.py.30.090192.001221. [DOI] [PubMed] [Google Scholar]
  18. Jacobson D. J. Control of mating type heterokaryon incompatibility by the tol gene in Neurospora crassa and N. tetrasperma. Genome. 1992 Apr;35(2):347–353. doi: 10.1139/g92-053. [DOI] [PubMed] [Google Scholar]
  19. Javerzat J. P., Bhattacherjee V., Barreau C. Isolation of telomeric DNA from the filamentous fungus Podospora anserina and construction of a self-replicating linear plasmid showing high transformation frequency. Nucleic Acids Res. 1993 Feb 11;21(3):497–504. doi: 10.1093/nar/21.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lecellier G., Silar P. Rapid methods for nucleic acids extraction from Petri dish-grown mycelia. Curr Genet. 1994 Feb;25(2):122–123. doi: 10.1007/BF00309536. [DOI] [PubMed] [Google Scholar]
  21. Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
  22. Loubradou G., Bégueret J., Turcq B. A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina. Genetics. 1997 Oct;147(2):581–588. doi: 10.1093/genetics/147.2.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Loubradou G., Bégueret J., Turcq B. An additional copy of the adenylate cyclase-encoding gene relieves developmental defects produced by a mutation in a vegetative incompatibility-controlling gene in Podospora anserina. Gene. 1996 Apr 17;170(1):119–123. doi: 10.1016/0378-1119(95)00847-0. [DOI] [PubMed] [Google Scholar]
  24. Orbach M. J. A cosmid with a HyR marker for fungal library construction and screening. Gene. 1994 Dec 2;150(1):159–162. doi: 10.1016/0378-1119(94)90877-x. [DOI] [PubMed] [Google Scholar]
  25. Philley M. L., Staben C. Functional analyses of the Neurospora crassa MT a-1 mating type polypeptide. Genetics. 1994 Jul;137(3):715–722. doi: 10.1093/genetics/137.3.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Punt P. J., Oliver R. P., Dingemanse M. A., Pouwels P. H., van den Hondel C. A. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene. 1987;56(1):117–124. doi: 10.1016/0378-1119(87)90164-8. [DOI] [PubMed] [Google Scholar]
  27. Ren R., Mayer B. J., Cicchetti P., Baltimore D. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 1993 Feb 19;259(5098):1157–1161. doi: 10.1126/science.8438166. [DOI] [PubMed] [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Saupe S. J., Kuldau G. A., Smith M. L., Glass N. L. The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics. 1996 Aug;143(4):1589–1600. doi: 10.1093/genetics/143.4.1589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Saupe S., Stenberg L., Shiu K. T., Griffiths A. J., Glass N. L. The molecular nature of mutations in the mt A-1 gene of the Neurospora crassa A idiomorph and their relation to mating-type function. Mol Gen Genet. 1996 Jan 15;250(1):115–122. doi: 10.1007/BF02191831. [DOI] [PubMed] [Google Scholar]
  31. Saupe S., Turcq B., Bégueret J. 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. 1995 Aug 30;162(1):135–139. doi: 10.1016/0378-1119(95)00272-8. [DOI] [PubMed] [Google Scholar]
  32. Turcq B., Bégueret J. The ura5 gene of the filamentous fungus Podospora anserina: nucleotide sequence and expression in transformed strains. Gene. 1987;53(2-3):201–209. doi: 10.1016/0378-1119(87)90008-4. [DOI] [PubMed] [Google Scholar]
  33. Vellani T. S., Griffiths A. J., Glass N. L. New mutations that suppress mating-type vegetative incompatibility in Neurospora crassa. Genome. 1994 Apr;37(2):249–255. doi: 10.1139/g94-035. [DOI] [PubMed] [Google Scholar]
  34. Yu H., Chen J. K., Feng S., Dalgarno D. C., Brauer A. W., Schreiber S. L. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell. 1994 Mar 11;76(5):933–945. doi: 10.1016/0092-8674(94)90367-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES