• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Feb 1999; 151(2): 545–555.
PMCID: PMC1460514

Molecular characterization of tol, a mediator of mating-type-associated vegetative incompatibility in Neurospora crassa.

Abstract

The mating-type locus in the haploid filamentous fungus, Neurospora crassa, controls mating and sexual development. The fusion of reproductive structures of opposite mating type, A and a, is required to initiate sexual reproduction. However, the fusion of hyphae of opposite mating type during vegetative growth results in growth inhibition and cell death, a process that is mediated by the tol locus. Mutations in tol are recessive and suppress mating-type-associated heterokaryon incompatibility. In this study, we describe the cloning and characterization of tol. The tol gene encodes a putative 1011-amino-acid polypeptide with a coiled-coil domain and a leucine-rich repeat. Both regions are required for tol activity. Repeat-induced point mutations in tol result in mutants that are wild type during vegetative growth and sexual reproduction, but that allow opposite mating-type individuals to form a vigorous heterokaryon. Transcript analyses show that tol mRNA is present during vegetative growth but absent during a cross. These data suggest that tol transcription is repressed to allow the coexistence of opposite mating-type nuclei during the sexual reproductive phase. tol is expressed in a mat A, mat a, A/a partial diploid and in a mating-type deletion strain, indicating that MAT A-1 and MAT a-1 are not absolutely required for transcription or repression of tol. These data suggest that TOL may rather interact with MAT A-1 and/or MAT a-1 (or downstream products) to form a death-triggering complex.

Full Text

The Full Text of this article is available as a PDF (310K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Beadle GW, Coonradt VL. Heterocaryosis in Neurospora Crassa. Genetics. 1944 May;29(3):291–308. [PMC free article] [PubMed]
  • Bégueret J, Turcq B, Clavé C. Vegetative incompatibility in filamentous fungi: het genes begin to talk. Trends Genet. 1994 Dec;10(12):441–446. [PubMed]
  • Buchanan SG, Gay NJ. Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol. 1996;65(1-2):1–44. [PubMed]
  • Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol. 1990 Apr 20;212(4):563–578. [PubMed]
  • Caten CE. Vegetative incompatibility and cytoplasmic infection in fungi. J Gen Microbiol. 1972 Sep;72(2):221–229. [PubMed]
  • Chen H, Kinsey JA. Purification of a heteromeric CCAAT binding protein from Neurospora crassa. Mol Gen Genet. 1995 Nov 27;249(3):301–308. [PubMed]
  • Chou PY, Fasman GD. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. [PubMed]
  • Debets F, Yang X, Griffiths AJ. 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. [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Ferreira AV, Saupe S, Glass NL. 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. [PubMed]
  • Ferreira AV, An Z, Metzenberg RL, Glass NL. Characterization of mat A-2, mat A-3 and deltamatA mating-type mutants of Neurospora crassa. Genetics. 1998 Mar;148(3):1069–1079. [PMC free article] [PubMed]
  • Garnier J, Osguthorpe DJ, Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. [PubMed]
  • Glass NL, Kuldau GA. Mating type and vegetative incompatibility in filamentous ascomycetes. Annu Rev Phytopathol. 1992;30:201–224. [PubMed]
  • Glass NL, Lee L. Isolation of Neurospora crassa A mating type mutants by repeat induced point (RIP) mutation. Genetics. 1992 Sep;132(1):125–133. [PMC free article] [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Glass NL, Grotelueschen J, Metzenberg RL. Neurospora crassa A mating-type region. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4912–4916. [PMC free article] [PubMed]
  • Anagnostakis SL. Biological control of chestnut blight. Science. 1982 Jan 29;215(4532):466–471. [PubMed]
  • Barreau C, Iskandar M, Loubradou G, Levallois V, Bégueret J. The mod-A suppressor of nonallelic heterokaryon incompatibility in Podospora anserina encodes a proline-rich polypeptide involved in female organ formation. Genetics. 1998 Jun;149(2):915–926. [PMC free article] [PubMed]
  • Griffiths AJ, Delange AM. Mutations of the a Mating-Type Gene in NEUROSPORA CRASSA. Genetics. 1978 Feb;88(2):239–254. [PMC free article] [PubMed]
  • Harbury PB, Zhang T, Kim PS, Alber T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science. 1993 Nov 26;262(5138):1401–1407. [PubMed]
  • Newmeyer D. A suppressor of the heterokaryon-incompatibility associated with mating type in Neurospora crassa. Can J Genet Cytol. 1970 Dec;12(4):914–926. [PubMed]
  • Hickey MJ, Williams SA, Roth GJ. Human platelet glycoprotein IX: an adhesive prototype of leucine-rich glycoproteins with flank-center-flank structures. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6773–6777. [PMC free article] [PubMed]
  • Noris P, Simsek S, Stibbe J, von dem Borne AE. A phenylalanine-55 to serine amino-acid substitution in the human glycoprotein IX leucine-rich repeat is associated with Bernard-Soulier syndrome. Br J Haematol. 1997 May;97(2):312–320. [PubMed]
  • Jacobson DJ. Control of mating type heterokaryon incompatibility by the tol gene in Neurospora crassa and N. tetrasperma. Genome. 1992 Apr;35(2):347–353. [PubMed]
  • Oakley CE, Weil CF, Kretz PL, Oakley BR. Cloning of the riboB locus of Aspergillus nidulans. Gene. 1987;53(2-3):293–298. [PubMed]
  • Orbach MJ. A cosmid with a HyR marker for fungal library construction and screening. Gene. 1994 Dec 2;150(1):159–162. [PubMed]
  • PAULING L, COREY RB. The structure of synthetic polypeptides. Proc Natl Acad Sci U S A. 1951 May;37(5):241–250. [PMC free article] [PubMed]
  • Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Kwon KJ, Raper KB. Heterokaryon formation and genetic analyses of color mutants in Aspergillus heterothallicus. Am J Bot. 1967 Jan;54(1):49–60. [PubMed]
  • Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. [PubMed]
  • Leslie JF. Fungal vegetative compatibility. Annu Rev Phytopathol. 1993;31:127–150. [PubMed]
  • Perkins DD, Barry EG. The cytogenetics of Neurospora. Adv Genet. 1977;19:133–285. [PubMed]
  • Leslie JF, Yamashiro CT. Effects of the tol mutation on allelic interactions at het loci in Neurospora crassa. Genome. 1997 Dec;40(6):834–840. [PubMed]
  • Philley ML, Staben C. Functional analyses of the Neurospora crassa MT a-1 mating type polypeptide. Genetics. 1994 Jul;137(3):715–722. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Raju NB. Meiosis and ascospore genesis in Neurospora. Eur J Cell Biol. 1980 Dec;23(1):208–223. [PubMed]
  • Lopez JA, Chung DW, Fujikawa K, Hagen FS, Davie EW, Roth GJ. The alpha and beta chains of human platelet glycoprotein Ib are both transmembrane proteins containing a leucine-rich amino acid sequence. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2135–2139. [PMC free article] [PubMed]
  • Saupe S, Stenberg L, Shiu KT, Griffiths AJ, Glass NL. 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. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Schweizer M, Case ME, Dykstra CC, Giles NH, Kushner SR. 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. [PMC free article] [PubMed]
  • Lumb KJ, Kim PS. A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry. 1995 Jul 11;34(27):8642–8648. [PubMed]
  • Lupas A. Coiled coils: new structures and new functions. Trends Biochem Sci. 1996 Oct;21(10):375–382. [PubMed]
  • Selker EU. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet. 1990;24:579–613. [PubMed]
  • Lupas A, Van Dyke M, Stock J. Predicting coiled coils from protein sequences. Science. 1991 May 24;252(5009):1162–1164. [PubMed]
  • Staben C, Yanofsky C. Neurospora crassa a mating-type region. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4917–4921. [PMC free article] [PubMed]
  • Malim MH, Böhnlein S, Hauber J, Cullen BR. Functional dissection of the HIV-1 Rev trans-activator--derivation of a trans-dominant repressor of Rev function. Cell. 1989 Jul 14;58(1):205–214. [PubMed]
  • van Diepeningen AD, Debets AJ, Hoekstra RF. Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet. 1997 Sep;32(3):209–217. [PubMed]
  • Metzenberg RL, Ahlgren SK. Behaviour of Neurospora tetrasperma mating-type genes introgressed into N. crassa. Can J Genet Cytol. 1973 Sep;15(3):571–576. [PubMed]
  • Vellani TS, Griffiths AJ, Glass NL. New mutations that suppress mating-type vegetative incompatibility in Neurospora crassa. Genome. 1994 Apr;37(2):249–255. [PubMed]
  • Metzenberg RL, Stevens JN, Selker EU, Morzycka-Wroblewska E. Identification and chromosomal distribution of 5S rRNA genes in Neurospora crassa. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2067–2071. [PMC free article] [PubMed]
  • Vollmer SJ, Yanofsky C. Efficient cloning of genes of Neurospora crassa. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4869–4873. [PMC free article] [PubMed]
  • Mindrinos M, Katagiri F, Yu GL, Ausubel FM. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 1994 Sep 23;78(6):1089–1099. [PubMed]
  • Mylyk OM. Heteromorphism for Heterokaryon Incompatibility Genes in Natural Populations of NEUROSPORA CRASSA. Genetics. 1976 Jun;83(2):275–284. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...