Home LiteratureArticle Details
PMID: 9529887 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Molecular genetics of mating recognition in basidiomycete fungi.

Microbiology and molecular biology reviews : MMBR ·Vol. 62 ·No. 1 ·1998-03-00 ·Pages 55-70

Casselton LA, Olesnicky NS

Abstract

The recognition of compatible mating partners in the basidiomycete fungi requires the coordinated activities of two gene complexes defined as the mating-type genes. One complex encodes members of the homeobox family of transcription factors, which heterodimerize on mating to generate an active transcription regulator. The other complex encodes peptide pheromones and 7-transmembrane receptors that permit intercellular signalling. Remarkably, a single species may have many thousands of cross-compatible mating types because the mating-type genes are multiallelic. Different alleles of both sets of genes are necessary for mating compatibility, and they trigger the initial stages of sexual development--the formation of a specialized filamentous mycelium termed the dikaryon, in which the haploid nuclei remain closely associated in each cell but do not fuse. Three species have been taken as models to describe the molecular structure and organization of the mating-type loci and the genes sequestered within them: the pathogenic smut fungus Ustilago maydis and the mushrooms Coprinus cinereus and Schizophyllum commune. Topics addressed in this review are the roles of the mating-type gene products in regulating sexual development, the molecular basis for multiple mating types, and the molecular interactions that permit different allelic products of the mating type genes to be discriminated. Attention is drawn to the remarkable conservation in the mechanisms that regulate sexual development in basidiomycetes and unicellular ascomycete yeasts, Saccharomyces cerevisiae and Schizosaccharomyces pombe, a theme which is developed in the general conclusion to include the filamentous ascomycetes Neurospora crassa and Podospora anserina.

MeSH Terms
Amino Acid Sequence Basidiomycota/physiology Genes, Fungal/physiology Genes, Homeobox/physiology Genes, Mating Type, Fungal Molecular Sequence Data Pheromones/physiology Reproduction Signal Transduction/physiology
Chemicals
Pheromones
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Casselton L A
Department of Plant Sciences, University of Oxford, United Kingdom. lcasselt@worf.molbiol.ox.ac.uk
Olesnicky N S
References (107)
107 references, click to expand
  1. Interaction between two homeodomain proteins is specified by a short C-terminal tail.
    Nature. 1994 Sep 29;371(6496):429-32 PMID: 8090224
  2. Control of mating and development in Ustilago maydis.
    Curr Opin Genet Dev. 1995 Oct;5(5):559-64 PMID: 8664542
  3. The pheromone response pathway in Saccharomyces cerevisiae.
    Annu Rev Genet. 1993;27:147-79 PMID: 8122900
  4. Structure of rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides.
    Biochem Biophys Res Commun. 1978 Aug 14;83(3):1077-83 PMID: 708426
  5. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5878-82 PMID: 16594058
  6. Heterodimerization between two classes of homeodomain proteins in the mushroom Coprinus cinereus brings together potential DNA-binding and activation domains.
    Gene. 1996 Jun 12;172(1):25-31 PMID: 8654986
  7. Ustilago maydis, the delightful blight.
    Trends Genet. 1992 May;8(5):174-80 PMID: 1369743
  8. A chimeric homeodomain protein causes self-compatibility and constitutive sexual development in the mushroom Coprinus cinereus.
    EMBO J. 1994 Sep 1;13(17):4054-9 PMID: 7915674
  9. The a mating type locus of U. maydis specifies cell signaling components.
    Cell. 1992 Feb 7;68(3):441-50 PMID: 1310895
  10. Pheromone signalling and polarized morphogenesis in yeast.
    Curr Opin Genet Dev. 1997 Feb;7(1):59-66 PMID: 9024634
  11. The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif.
    Cell. 1990 Jan 26;60(2):295-306 PMID: 1967554
  12. The mating-type locus B alpha 1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes.
    EMBO J. 1995 Nov 1;14(21):5271-8 PMID: 7489716
  13. The mat- allele of Podospora anserina contains three regulatory genes required for the development of fertilized female organs.
    Mol Gen Genet. 1993 Dec;241(5-6):667-73 PMID: 8264541
  14. Molecular analysis of the Coprinus cinereus mating type A factor demonstrates an unexpectedly complex structure.
    Genetics. 1991 Jul;128(3):529-38 PMID: 1678725
  15. Cell-type-specific transcription in yeast.
    Biochim Biophys Acta. 1991 Feb 16;1088(2):155-69 PMID: 1900437
  16. Mechanism of specificity in the Fos-Jun oncoprotein heterodimer.
    Cell. 1992 Feb 21;68(4):699-708 PMID: 1739975
  17. STE12, a protein involved in cell-type-specific transcription and signal transduction in yeast, is part of protein-DNA complexes.
    Genes Dev. 1989 Sep;3(9):1349-61 PMID: 2558054
  18. Cell differentiation by interaction of two HMG-box proteins: Mat1-Mc activates M cell-specific genes in S.pombe by recruiting the ubiquitous transcription factor Ste11 to weak binding sites.
    EMBO J. 1997 Jul 1;16(13):4021-33 PMID: 9233811
  19. A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an alpha 2 dimer.
    Cell. 1992 Jan 10;68(1):133-42 PMID: 1732062
  20. The carboxy-terminal tail of the homeo domain protein alpha 2 is required for function with a second homeo domain protein.
    Genes Dev. 1993 Oct;7(10):1862-70 PMID: 8104845
  21. Interactions of coiled coils in transcription factors: where is the specificity?
    Curr Opin Genet Dev. 1993 Apr;3(2):278-85 PMID: 8504253
  22. Alpha-helical coiled coils and bundles: how to design an alpha-helical protein.
    Proteins. 1990;7(1):1-15 PMID: 2184436
  23. Constitutively active mutants of the alpha 1B-adrenergic receptor: role of highly conserved polar amino acids in receptor activation.
    EMBO J. 1996 Jul 15;15(14):3566-78 PMID: 8670860
  24. A fungal mating type protein that regulates sexual and asexual development contains a POU-related domain.
    EMBO J. 1992 May;11(5):1805-13 PMID: 1582410
  25. Crystal structure of the MATa1/MAT alpha 2 homeodomain heterodimer bound to DNA.
    Science. 1995 Oct 13;270(5234):262-9 PMID: 7569974
  26. The Two Nuclei in the Dikaryon of the Homobasidiomycete Coprinus cinereus Change Position after Each Conjugate Division
    Fungal Genet Biol. 1998 Feb;23(1):110-6 PMID: 9514693
  27. The Structure of the a Mating Type Locus in Coprinus Lagopus.
    Genetics. 1960 May;45(5):641-50 PMID: 17247950
  28. Coiled coils: new structures and new functions.
    Trends Biochem Sci. 1996 Oct;21(10):375-82 PMID: 8918191
  29. Conservation of the b mating-type gene complex among bipolar and tetrapolar smut fungi.
    Plant Cell. 1993 Jan;5(1):123-36 PMID: 8439742
  30. The homeodomains of the heterodimeric bE and bW proteins of Ustilago maydis are both critical for function.
    Mol Gen Genet. 1997 May 20;254(5):514-9 PMID: 9197410
  31. An N-Terminal Dimerization Domain Permits Homeodomain Proteins To Choose Compatible Partners and Initiate Sexual Development in the Mushroom Coprinus cinereus.
    Plant Cell. 1995 Jun;7(6):773-83 PMID: 12242384
  32. Homeodomains and regulation of sexual development in basidiomycetes.
    Trends Genet. 1992 May;8(5):154-5 PMID: 1369739
  33. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize.
    Annu Rev Genet. 1995;29:179-208 PMID: 8825473
  34. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7085-9 PMID: 7913746
  35. Functional coupling of a mammalian somatostatin receptor to the yeast pheromone response pathway.
    Mol Cell Biol. 1995 Nov;15(11):6188-95 PMID: 7565771
  36. Only one of the paired Schizophyllum commune A alpha mating-type, putative homeobox genes encodes a homeodomain essential for A alpha-regulated development.
    Mol Gen Genet. 1994 Aug 2;244(3):318-24 PMID: 7914671
  37. Comparison of two b1 alleles from within the A mating-type of the basidiomycete Coprinus cinereus.
    Gene. 1994 Sep 2;146(2):167-76 PMID: 8076815
  38. Defects in G protein-coupled signal transduction in human disease.
    Annu Rev Physiol. 1996;58:143-70 PMID: 8815789
  39. Homeobox genes and axial patterning.
    Cell. 1992 Jan 24;68(2):283-302 PMID: 1346368
  40. Interaction of the A alpha Y and Z mating-type homeodomain proteins of Schizophyllum commune detected by the two-hybrid system.
    Biochem Biophys Res Commun. 1995 Jun 26;211(3):1071-6 PMID: 7598694
  41. Pheromones and pheromone receptors as mating-type determinants in basidiomycetes.
    Genet Eng (N Y). 1996;18:219-47 PMID: 8785123
  42. The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene.
    Mol Cell Biol. 1993 Mar;13(3):1962-70 PMID: 8441425
  43. Activating mutations of rhodopsin and other G protein-coupled receptors.
    Annu Rev Biophys Biomol Struct. 1996;25:287-314 PMID: 8800472
  44. Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins.
    Nature. 1984 Jul 5-11;310(5972):70-1 PMID: 6429549
  45. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures.
    Trends Genet. 1994 Mar;10(3):94-100 PMID: 8178371
  46. Life cycle of the budding yeast Saccharomyces cerevisiae.
    Microbiol Rev. 1988 Dec;52(4):536-53 PMID: 3070323
  47. Multiple genes encoding pheromones and a pheromone receptor define the B beta 1 mating-type specificity in Schizophyllum commune.
    Genetics. 1997 Jun;146(2):541-51 PMID: 9178005
  48. Mating pheromone-induced expression of the mat1-Pm gene of Schizosaccharomyces pombe: identification of signalling components and characterization of upstream controlling elements.
    Yeast. 1994 Jun;10(6):757-70 PMID: 7975894
  49. The b mating-type locus of Ustilago maydis contains variable and constant regions.
    Genes Dev. 1990 Aug;4(8):1384-95 PMID: 2227416
  50. Pheromones trigger filamentous growth in Ustilago maydis.
    EMBO J. 1994 Apr 1;13(7):1620-7 PMID: 8157001
  51. Functional analysis of the homeodomain-related proteins of the A alpha locus of Schizophyllum commune.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7174-8 PMID: 1353887
  52. Identification of the pheromone response element in Ustilago maydis.
    Mol Gen Genet. 1996 Apr 24;251(1):31-7 PMID: 8628244
  53. The A mating-type genes of the mushroom Coprinus cinereus are not differentially transcribed in monokaryons and dikaryons.
    Mol Gen Genet. 1993 Apr;238(1-2):304-7 PMID: 8479436
  54. Correlation of genetic and physical maps at the A mating-type locus of Coprinus cinereus.
    Genetics. 1996 Dec;144(4):1471-7 PMID: 8978036
  55. G proteins in Ustilago maydis: transmission of multiple signals?
    EMBO J. 1997 Apr 15;16(8):1934-42 PMID: 9155019
  56. The genetic structure of the incompatibility factors of Schizophyllum commune: comparative studies of primary mutations in the B factor.
    Mol Gen Genet. 1968;102(3):196-203 PMID: 5751823
  57. The Schizosaccharomyces pombe map1 gene encodes an SRF/MCM1-related protein required for P-cell specific gene expression.
    Mol Gen Genet. 1996 Dec 13;253(3):387-92 PMID: 9003326
  58. Four mating-type genes control sexual differentiation in the fission yeast.
    EMBO J. 1988 May;7(5):1537-47 PMID: 2900761
  59. Signal transduction during pheromone response in yeast.
    Annu Rev Cell Biol. 1991;7:699-728 PMID: 1667085
  60. Pheromone-dependent phosphorylation of the yeast STE12 protein correlates with transcriptional activation.
    Genes Dev. 1991 May;5(5):741-50 PMID: 2026326
  61. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein.
    Nature. 1989 Aug 3;340(6232):400-4 PMID: 2569166
  62. Molecular mechanisms of cell-type determination in budding yeast.
    Curr Opin Genet Dev. 1995 Oct;5(5):552-8 PMID: 8664541
  63. Dikaryosis: genetic determination in Schizophyllum.
    Science. 1968 Apr 5;160(3823):85-6 PMID: 5642314
  64. Mutational analysis of natural alleles in and affecting the B incompatibility factor of Schizophyllum.
    Genetics. 1979 Oct;93(2):383-91 PMID: 575338
  65. A point mutation in the glucose-dependent insulinotropic peptide receptor confers constitutive activity.
    Biochem Biophys Res Commun. 1997 Mar 6;232(1):96-100 PMID: 9125160
  66. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis.
    Cell. 1995 Apr 7;81(1):73-83 PMID: 7720075
  67. Primary and secondary mutations at the incompatibility loci in Schizophyllum.
    Proc Natl Acad Sci U S A. 1965 Jun;53(6):1324-32 PMID: 5217634
  68. Mapping the heterogeneous DNA region that determines the nine A alpha mating-type specificities of Schizophyllum commune.
    Genetics. 1994 Jul;137(3):709-14 PMID: 8088516
  69. THE GENETIC STRUCTURE OF THE INCOMPATIBILITY FACTORS OF SCHIZOPHYLLUM COMMUNE: THE A-FACTOR.
    Proc Natl Acad Sci U S A. 1960 Jun;46(6):833-42 PMID: 16590680
  70. Mutations in the B incompatibility factor of Schizophyllum commune.
    Proc Natl Acad Sci U S A. 1962 May 15;48:743-50 PMID: 14483788
  71. Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes.
    Genetics. 1996 Sep;144(1):87-94 PMID: 8878675
  72. Gbeta subunit interacts with a peptide encoding region 956-982 of adenylyl cyclase 2. Cross-linking of the peptide to free Gbetagamma but not the heterotrimer.
    J Biol Chem. 1996 Oct 25;271(43):26445-8 PMID: 8900107
  73. Direct studies of dikaryotization in Schizophyllum commune. I. Live inter-cellular nuclear migration patterns.
    Arch Microbiol. 1980 Dec;128(2):162-71 PMID: 7011241
  74. Properties of the DNA-binding domain of the Saccharomyces cerevisiae STE12 protein.
    Mol Cell Biol. 1991 Dec;11(12):5910-8 PMID: 1944269
  75. Two classes of homeodomain proteins specify the multiple a mating types of the mushroom Coprinus cinereus.
    Plant Cell. 1994 Oct;6(10):1467-75 PMID: 7994179
  76. Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation.
    Microbiol Rev. 1995 Sep;59(3):406-22 PMID: 7565412
  77. Noncontiguous domains of the alpha-factor receptor of yeasts confer ligand specificity.
    J Biol Chem. 1994 Jan 14;269(2):968-73 PMID: 8288649
  78. A two-component regulatory system for self/non-self recognition in Ustilago maydis.
    Cell. 1992 Feb 21;68(4):647-57 PMID: 1739973
  79. Hormonal stimulation of adenylyl cyclase through Gi-protein beta gamma subunits.
    Nature. 1992 Mar 12;356(6365):159-61 PMID: 1312225
  80. Cloning and characterization of a Schizophyllum gene with A beta 6 mating-type activity.
    Curr Genet. 1996 Jan;29(2):136-42 PMID: 8821660
  81. The A alpha mating locus of Schizophyllum commune encodes two dissimilar multiallelic homeodomain proteins.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7169-73 PMID: 1353886
  82. Signalling enzymes: bursting with potential.
    Curr Biol. 1997 Aug 1;7(8):R470-3 PMID: 9259544
  83. Isolation and characterization of a gene encoding a G-protein alpha subunit from Schizosaccharomyces pombe: involvement in mating and sporulation pathways.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5877-81 PMID: 1905818
  84. The Schizosaccharomyces pombe mating-type gene mat-Mc encodes a sequence-specific DNA-binding high mobility group box protein.
    J Biol Chem. 1993 Nov 25;268(33):24813-7 PMID: 8227043
  85. Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle.
    Genes Dev. 1994 Jun 15;8(12):1367-78 PMID: 7926737
  86. Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells.
    EMBO J. 1989 Dec 20;8(13):3973-84 PMID: 2686977
  87. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis.
    EMBO J. 1996 Apr 1;15(7):1632-41 PMID: 8612587
  88. Pharmacology of a constitutively active muscarinic receptor generated by random mutagenesis.
    J Pharmacol Exp Ther. 1995 Dec;275(3):1274-9 PMID: 8531092
  89. Altered mating-type identity in the fungus Podospora anserina leads to selfish nuclei, uniparental progeny, and haploid meiosis.
    Genetics. 1995 Jun;140(2):493-503 PMID: 7498731
  90. Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development.
    Genes Dev. 1991 Nov;5(11):1990-9 PMID: 1657709
  91. The formation of diploids of Ustilago maydis on agar medium.
    Phytopathology. 1969 Nov;59(11):1771-2 PMID: 5377745
  92. Construction of chimeric alleles with altered specificity at the b incompatibility locus of Ustilago maydis.
    Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):664-8 PMID: 8421703
  93. Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7762-6 PMID: 8052657
  94. How receptors talk to trimeric G proteins.
    Curr Opin Cell Biol. 1997 Apr;9(2):134-42 PMID: 9069253
  95. The Incompatibility Factors and a Related Gene in Schizophyllum Commune.
    Genetics. 1951 Sep;36(5):441-59 PMID: 17247358
  96. Somatostatin receptor-mediated signaling in smooth muscle. Activation of phospholipase C-beta3 by Gbetagamma and inhibition of adenylyl cyclase by Galphai1 and Galphao.
    J Biol Chem. 1996 Sep 20;271(38):23458-63 PMID: 8798553
  97. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus.
    Genetics. 1998 Mar;148(3):1081-90 PMID: 9539426
  98. The yeast STE12 protein binds to the DNA sequence mediating pheromone induction.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5703-7 PMID: 2668945
  99. Role of a cell-wall glucan-degrading enzyme in mating of Schizophyllum commune.
    J Bacteriol. 1967 Nov;94(5):1594-602 PMID: 6057808
  100. Ssn6-Tup1 is a general repressor of transcription in yeast.
    Cell. 1992 Feb 21;68(4):709-19 PMID: 1739976
  101. The combination of dissimilar alleles of the A alpha and A beta gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus.
    Genes Dev. 1992 Apr;6(4):568-77 PMID: 1348484
  102. The specificity determinant of the Y mating-type proteins of Schizophyllum commune is also essential for Y-Z protein binding.
    Genetics. 1997 Feb;145(2):253-60 PMID: 9071581
  103. Investigation of growth hormone releasing hormone receptor structure and activity using yeast expression technologies.
    J Recept Signal Transduct Res. 1997 Jan-May;17(1-3):293-303 PMID: 9029497
  104. Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources
    Fungal Genet Biol. 1996 Dec;20(4):299-312 PMID: 9045760
  105. Signalling in the yeasts: an informational cascade with links to the filamentous fungi.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):249-74 PMID: 9618441
  106. Sexual pheromones and mating responses in fungi.
    Plant Cell. 1993 Oct;5(10):1461-9 PMID: 8281042
  107. Homeodomain-DNA recognition.
    Cell. 1994 Jul 29;78(2):211-23 PMID: 8044836
Article Info
Journal
Microbiology and molecular biology reviews : MMBR
Abbr.
Microbiol Mol Biol Rev
ISSN
1092-2172
Published
1998-03-00
Pages
55-70
Language
English
Region
United States
NLM ID
9706653
PMCID
PMC98906
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com