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. 1996 Aug;143(4):1589–1600. doi: 10.1093/genetics/143.4.1589

The Product of the Het-C Heterokaryon Incompatibility Gene of Neurospora Crassa Has Characteristics of a Glycine-Rich Cell Wall Protein

S J Saupe 1, G A Kuldau 1, M L Smith 1, N L Glass 1
PMCID: PMC1207423  PMID: 8844148

Abstract

Filamentous fungi are capable of hyphal fusion, but heterokaryon formation between different isolates is controlled by specific loci termed het loci. Heterokaryotic cells formed between strains of different het genotype are rapidly destroyed or strongly inhibited in their growth. In Neurospora crassa, at least 11 loci, including the mating type locus, affect the capacity to form a heterokaryon between different isolates. In this report, we describe the molecular characterization of the vegetative incompatibility locus, het-C. The het-C(OR) allele was cloned by genetically identifying the het-C locus in a chromosome walk, and the activity of clones containing the het-C(OR) allele was tested in a functional transformation assay. The het-C(OR) allele encodes a 966-amino acid polypeptide with a putative signal peptide, a coiled-coil motif and a C-terminal glycine-rich domain, similar to glycine-rich domains detected in various extracellular and structural cell envelope proteins. Both the coiled-coil and one-third of the glycine-rich carboxyl terminal domains were required for full het-C(OR) activity. Mutants of het-C(OR) were obtained by repeat-induced point mutation (RIP); these mutants were indistinguishable from wild type during vegetative growth and sexual reproduction but displayed dual compatibility with both of two mutually incompatible het-C(OR) and het-c(PA) strains.

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Selected References

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  1. 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]
  2. Beadle G W, Coonradt V L. Heterocaryosis in Neurospora Crassa. Genetics. 1944 May;29(3):291–308. doi: 10.1093/genetics/29.3.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bobek L., Rekosh D. M., van Keulen H., LoVerde P. T. Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5544–5548. doi: 10.1073/pnas.83.15.5544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buxton F. P., Radford A. Cloning of the structural gene for orotidine 5'-phosphate carboxylase of Neurospora crassa by expression in Escherichia coli. Mol Gen Genet. 1983;190(3):403–405. doi: 10.1007/BF00331067. [DOI] [PubMed] [Google Scholar]
  5. Ferreira A. V., Saupe S., Glass N. L. Transcriptional analysis of the mtA idiomorph of Neurospora crassa identifies two genes in addition to mtA-1. Mol Gen Genet. 1996 Apr 10;250(6):767–774. doi: 10.1007/BF02172989. [DOI] [PubMed] [Google Scholar]
  6. Fuchs E., Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem. 1994;63:345–382. doi: 10.1146/annurev.bi.63.070194.002021. [DOI] [PubMed] [Google Scholar]
  7. Garnjobst L., Wilson J. F. HETEROCARYOSIS AND PROTOPLASMIC INCOMPATIBILITY IN NEUROSPORA CRASSA. Proc Natl Acad Sci U S A. 1956 Sep;42(9):613–618. doi: 10.1073/pnas.42.9.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gierasch L. M. Signal sequences. Biochemistry. 1989 Feb 7;28(3):923–930. doi: 10.1021/bi00429a001. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Glass N. L., Vollmer S. J., Staben C., Grotelueschen J., Metzenberg R. L., Yanofsky C. DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science. 1988 Jul 29;241(4865):570–573. doi: 10.1126/science.2840740. [DOI] [PubMed] [Google Scholar]
  11. Ho C. Y., Adamson J. G., Hodges R. S., Smith M. Heterodimerization of the yeast MATa1 and MAT alpha 2 proteins is mediated by two leucine zipper-like coiled-coil motifs. EMBO J. 1994 Mar 15;13(6):1403–1413. doi: 10.1002/j.1460-2075.1994.tb06394.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
  13. Mehrel T., Hohl D., Rothnagel J. A., Longley M. A., Bundman D., Cheng C., Lichti U., Bisher M. E., Steven A. C., Steinert P. M. Identification of a major keratinocyte cell envelope protein, loricrin. Cell. 1990 Jun 15;61(6):1103–1112. doi: 10.1016/0092-8674(90)90073-n. [DOI] [PubMed] [Google Scholar]
  14. Mishra N. C. Genetics and biochemistry of morphogenesis in Neurospora. Adv Genet. 1977;19:341–405. doi: 10.1016/s0065-2660(08)60248-5. [DOI] [PubMed] [Google Scholar]
  15. Mylyk O. M. Heterokaryon incompatibility genes in Neurospora crassa detected using duplication-producing chromosome rearrangements. Genetics. 1975 May;80(1):107–124. doi: 10.1093/genetics/80.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nothwehr S. F., Gordon J. I. Eukaryotic signal peptide structure/function relationships. Identification of conformational features which influence the site and efficiency of co-translational proteolytic processing by site-directed mutagenesis of human pre(delta pro)apolipoprotein A-II. J Biol Chem. 1989 Mar 5;264(7):3979–3987. [PubMed] [Google Scholar]
  17. O'Shea E. K., Rutkowski R., Kim P. S. Mechanism of specificity in the Fos-Jun oncoprotein heterodimer. Cell. 1992 Feb 21;68(4):699–708. doi: 10.1016/0092-8674(92)90145-3. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Pabo C. O., Sauer R. T. Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem. 1992;61:1053–1095. doi: 10.1146/annurev.bi.61.070192.005201. [DOI] [PubMed] [Google Scholar]
  20. Perkins D. D., Radford A., Newmeyer D., Björkman M. Chromosomal loci of Neurospora crassa. Microbiol Rev. 1982 Dec;46(4):426–570. doi: 10.1128/mr.46.4.426-570.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Perkins D. D. The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes in Neurospora. Genetics. 1975 May;80(1):87–105. doi: 10.1093/genetics/80.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Saupe S., Descamps C., Turcq B., Bégueret J. 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 U S A. 1994 Jun 21;91(13):5927–5931. doi: 10.1073/pnas.91.13.5927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Schweizer M., Case M. E., Dykstra C. C., Giles N. H., Kushner S. R. Identification and characterization of recombinant plasmids carrying the complete qa gene cluster from Neurospora crassa including the qa-1+ regulatory gene. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5086–5090. doi: 10.1073/pnas.78.8.5086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Selker E. U. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet. 1990;24:579–613. doi: 10.1146/annurev.ge.24.120190.003051. [DOI] [PubMed] [Google Scholar]
  26. Showalter A. M. Structure and function of plant cell wall proteins. Plant Cell. 1993 Jan;5(1):9–23. doi: 10.1105/tpc.5.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Singer M. J., Marcotte B. A., Selker E. U. DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol Cell Biol. 1995 Oct;15(10):5586–5597. doi: 10.1128/mcb.15.10.5586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Staben C., Yanofsky C. Neurospora crassa a mating-type region. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4917–4921. doi: 10.1073/pnas.87.13.4917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steinert P. M., Mack J. W., Korge B. P., Gan S. Q., Haynes S. R., Steven A. C. Glycine loops in proteins: their occurrence in certain intermediate filament chains, loricrins and single-stranded RNA binding proteins. Int J Biol Macromol. 1991 Jun;13(3):130–139. doi: 10.1016/0141-8130(91)90037-u. [DOI] [PubMed] [Google Scholar]
  30. Turcq B., Deleu C., Denayrolles M., Bégueret J. Two allelic genes responsible for vegetative incompatibility in the fungus Podospora anserina are not essential for cell viability. Mol Gen Genet. 1991 Aug;228(1-2):265–269. doi: 10.1007/BF00282475. [DOI] [PubMed] [Google Scholar]
  31. de Bruijn F. J., Lupski J. R. The use of transposon Tn5 mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids--a review. Gene. 1984 Feb;27(2):131–149. doi: 10.1016/0378-1119(84)90135-5. [DOI] [PubMed] [Google Scholar]

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