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. 1994 Sep 1;13(17):4054–4059. doi: 10.1002/j.1460-2075.1994.tb06722.x

A chimeric homeodomain protein causes self-compatibility and constitutive sexual development in the mushroom Coprinus cinereus.

U Kües 1, B Göttgens 1, R Stratmann 1, W V Richardson 1, S F O'Shea 1, L A Casselton 1
PMCID: PMC395326  PMID: 7915674

Abstract

The A mating type genes of the mushroom Coprinus cinereus encode two classes of putative transcription factor with distinctive homeodomain motifs (HD1 and HD2). A successful mating brings together different allelic forms of these genes and this triggers part of a developmental sequence required for sexual reproduction. In this report we provide evidence that this developmental programme is promoted by a physical interaction between the two classes of homeodomain protein. Rare dominant mutations conferring self-compatibility map to the A locus and result in constitutive operation of the A-regulated developmental pathway. Our molecular analysis of one of these mutations shows that it has generated a chimeric gene by inframe fusion of an HD2 and an HD1 gene. Fusion has overcome the normal incompatibility between two proteins coded by genes of the same A locus and generated a protein that is sufficient to promote development in the absence of any other active A mating type genes. The fusion protein retains most of the HD2 sequence, but only the C-terminal part of the HD1 protein. It has only the HD2 homeodomain motif as a potential DNA binding domain fused to an essential C-terminal region of the HD1 protein, which in a normal HD1-HD2 protein complex may be the major activation domain.

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Selected References

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  1. Ananthan J., Baler R., Morrissey D., Zuo J., Lan Y., Weir M., Voellmy R. Synergistic activation of transcription is mediated by the N-terminal domain of Drosophila fushi tarazu homeoprotein and can occur without DNA binding by the protein. Mol Cell Biol. 1993 Mar;13(3):1599–1609. doi: 10.1128/mcb.13.3.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bakkeren G., Kronstad J. W. Conservation of the b mating-type gene complex among bipolar and tetrapolar smut fungi. Plant Cell. 1993 Jan;5(1):123–136. doi: 10.1105/tpc.5.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Binninger D. M., Skrzynia C., Pukkila P. J., Casselton L. A. DNA-mediated transformation of the basidiomycete Coprinus cinereus. EMBO J. 1987 Apr;6(4):835–840. doi: 10.1002/j.1460-2075.1987.tb04828.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cleary M. L. Oncogenic conversion of transcription factors by chromosomal translocations. Cell. 1991 Aug 23;66(4):619–622. doi: 10.1016/0092-8674(91)90105-8. [DOI] [PubMed] [Google Scholar]
  5. Day P R. The Structure of the a Mating Type Locus in Coprinus Lagopus. Genetics. 1960 May;45(5):641–650. doi: 10.1093/genetics/45.5.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dedera D. A., Waller E. K., LeBrun D. P., Sen-Majumdar A., Stevens M. E., Barsh G. S., Cleary M. L. Chimeric homeobox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell. 1993 Sep 10;74(5):833–843. doi: 10.1016/0092-8674(93)90463-z. [DOI] [PubMed] [Google Scholar]
  7. Dolan J. W., Fields S. Cell-type-specific transcription in yeast. Biochim Biophys Acta. 1991 Feb 16;1088(2):155–169. doi: 10.1016/0167-4781(91)90051-m. [DOI] [PubMed] [Google Scholar]
  8. Dranginis A. M. Binding of yeast a1 and alpha 2 as a heterodimer to the operator DNA of a haploid-specific gene. Nature. 1990 Oct 18;347(6294):682–685. doi: 10.1038/347682a0. [DOI] [PubMed] [Google Scholar]
  9. Fitzpatrick V. D., Percival-Smith A., Ingles C. J., Krause H. M. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature. 1992 Apr 16;356(6370):610–612. doi: 10.1038/356610a0. [DOI] [PubMed] [Google Scholar]
  10. Gillissen B., Bergemann J., Sandmann C., Schroeer B., Bölker M., Kahmann R. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell. 1992 Feb 21;68(4):647–657. doi: 10.1016/0092-8674(92)90141-x. [DOI] [PubMed] [Google Scholar]
  11. Goutte C., Johnson A. D. Recognition of a DNA operator by a dimer composed of two different homeodomain proteins. EMBO J. 1994 Mar 15;13(6):1434–1442. doi: 10.1002/j.1460-2075.1994.tb06397.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kamps M. P., Look A. T., Baltimore D. The human t(1;19) translocation in pre-B ALL produces multiple nuclear E2A-Pbx1 fusion proteins with differing transforming potentials. Genes Dev. 1991 Mar;5(3):358–368. doi: 10.1101/gad.5.3.358. [DOI] [PubMed] [Google Scholar]
  13. Kamps M. P., Murre C., Sun X. H., Baltimore D. A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell. 1990 Feb 23;60(4):547–555. doi: 10.1016/0092-8674(90)90658-2. [DOI] [PubMed] [Google Scholar]
  14. Kües U., Richardson W. V., Tymon A. M., Mutasa E. S., Göttgens B., Gaubatz S., Gregoriades A., Casselton L. A. 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):568–577. doi: 10.1101/gad.6.4.568. [DOI] [PubMed] [Google Scholar]
  15. Mak A., Johnson A. D. 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):1862–1870. doi: 10.1101/gad.7.10.1862. [DOI] [PubMed] [Google Scholar]
  16. May G., Le Chevanton L., Pukkila P. J. Molecular analysis of the Coprinus cinereus mating type A factor demonstrates an unexpectedly complex structure. Genetics. 1991 Jul;128(3):529–538. doi: 10.1093/genetics/128.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nourse J., Mellentin J. D., Galili N., Wilkinson J., Stanbridge E., Smith S. D., Cleary M. L. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell. 1990 Feb 23;60(4):535–545. doi: 10.1016/0092-8674(90)90657-z. [DOI] [PubMed] [Google Scholar]
  18. Nucifora G., Begy C. R., Erickson P., Drabkin H. A., Rowley J. D. The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER 1. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7784–7788. doi: 10.1073/pnas.90.16.7784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. PARAG Y. Mutations in the B incompatibility factor of Schizophyllum commune. Proc Natl Acad Sci U S A. 1962 May 15;48:743–750. doi: 10.1073/pnas.48.5.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pukkila P. J., Yashar B. M., Binninger D. M. Analysis of meiotic development in Coprinus cinereus. Symp Soc Exp Biol. 1984;38:177–194. [PubMed] [Google Scholar]
  21. Rao P. S., Niederpruem D. J. Carbohydrate metabolism during morphogenesis of Coprinus lagopus (sensu Buller). J Bacteriol. 1969 Dec;100(3):1222–1228. doi: 10.1128/jb.100.3.1222-1228.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Raper J. R., Boyd D. H., Raper C. A. Primary and secondary mutations at the incompatibility loci in Schizophyllum. Proc Natl Acad Sci U S A. 1965 Jun;53(6):1324–1332. doi: 10.1073/pnas.53.6.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Richardson W. V., Kües U., Casselton L. A. 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):304–307. doi: 10.1007/BF00279559. [DOI] [PubMed] [Google Scholar]
  24. Sealy-Lewis H. M., Casselton L. A. Restoration of enzyme activity by recessive missense suppressors in the fungus Coprinus. Mol Gen Genet. 1978 Aug 17;164(2):211–215. doi: 10.1007/BF00267386. [DOI] [PubMed] [Google Scholar]
  25. Specht C. A., Stankis M. M., Giasson L., Novotny C. P., Ullrich R. C. 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):7174–7178. doi: 10.1073/pnas.89.15.7174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tornow J., Zeng X., Gao W., Santangelo G. M. GCR1, a transcriptional activator in Saccharomyces cerevisiae, complexes with RAP1 and can function without its DNA binding domain. EMBO J. 1993 Jun;12(6):2431–2437. doi: 10.1002/j.1460-2075.1993.tb05897.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tymon A. M., Kües U., Richardson W. V., Casselton L. A. A fungal mating type protein that regulates sexual and asexual development contains a POU-related domain. EMBO J. 1992 May;11(5):1805–1813. doi: 10.1002/j.1460-2075.1992.tb05232.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yee A. R., Kronstad J. W. 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):664–668. doi: 10.1073/pnas.90.2.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. von Lindern M., Fornerod M., van Baal S., Jaegle M., de Wit T., Buijs A., Grosveld G. The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol Cell Biol. 1992 Apr;12(4):1687–1697. doi: 10.1128/mcb.12.4.1687. [DOI] [PMC free article] [PubMed] [Google Scholar]

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