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Tgs1 is the enzyme that converts m(7)G RNA caps to the 2,2,7-trimethylguanosine (TMG) caps characteristic of spliceosomal snRNAs. Fungi grow vegetatively without TMG caps, thereby raising the question of what cellular transactions, if any, are TMG cap-dependent. Here, we report that Saccharomyces cerevisiae Tgs1 methyltransferase activity is essential for meiosis. tgs1Δ cells are specifically defective in splicing PCH2 and SAE3 meiotic pre-mRNAs. The TMG requirement for SAE3 splicing is alleviated by two intron mutations: a UAUUAAC to UACUAAC change that restores a consensus branchpoint and disruption of a stem-loop encompassing the branchpoint. The TMG requirement for PCH2 splicing is alleviated by a CACUAAC to UACUAAC change restoring a consensus branchpoint and by shortening the PCH2 5' exon. Placing the SAE3 and PCH2 introns within a HIS3 reporter confers Tgs1-dependent histidine prototrophy, signifying that the respective introns are portable determinants of TMG-dependent gene expression. Analysis of in vitro splicing in extracts of TGS1 versus tgs1Δ cells showed that SAE3 intron removal was enfeebled without TMG caps, whereas splicing of ACT1 was unaffected. Our findings illuminate a new mode of tunable splicing, a reliance on TMG caps for an essential developmental RNA transaction, and three genetically distinct meiotic splicing regulons in budding yeast.

Titel:	An essential role for trimethylguanosine RNA caps in Saccharomyces cerevisiae meiosis and their requirement for splicing of SAE3 and PCH2 meiotic pre-mRNAs.
Autor/in / Beteiligte Person:	Qiu, ZR ; Shuman, S ; Schwer, B
Link:	Zum Volltext
Zeitschrift:	Nucleic acids research, Jg. 39 (2011-07-01), Heft 13, S. 5633-46
Veröffentlichung:	1992- : Oxford : Oxford University Press ; <i>Original Publication</i>: London, Information Retrieval ltd., 2011
Medientyp:	academicJournal
ISSN:	1362-4962 (electronic)
DOI:	10.1093/nar/gkr083
Schlagwort:	Endonucleases metabolism Exons Gene Deletion Guanosine analogs & derivatives Guanosine metabolism Introns Meiosis genetics Methyltransferases genetics Nuclear Proteins metabolism Nucleic Acid Conformation RNA Precursors metabolism RNA, Messenger chemistry RNA, Messenger metabolism RNA-Binding Proteins physiology Saccharomyces cerevisiae metabolism Saccharomyces cerevisiae physiology Saccharomyces cerevisiae Proteins metabolism Saccharomyces cerevisiae Proteins physiology Spores, Fungal enzymology Endonucleases genetics Methyltransferases physiology Nuclear Proteins genetics RNA Splicing Saccharomyces cerevisiae genetics Saccharomyces cerevisiae Proteins genetics
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article; Research Support, N.I.H., Extramural Language: English [Nucleic Acids Res] 2011 Jul; Vol. 39 (13), pp. 5633-46. <i>Date of Electronic Publication: </i>2011 Mar 11. MeSH Terms: RNA Splicing* ; Endonucleases / genetics ; Methyltransferases / physiology ; Nuclear Proteins / genetics ; Saccharomyces cerevisiae / genetics ; Saccharomyces cerevisiae Proteins / *genetics ; Endonucleases / metabolism ; Exons ; Gene Deletion ; Guanosine / analogs & derivatives ; Guanosine / metabolism ; Introns ; Meiosis / genetics ; Methyltransferases / genetics ; Nuclear Proteins / metabolism ; Nucleic Acid Conformation ; RNA Precursors / metabolism ; RNA, Messenger / chemistry ; RNA, Messenger / metabolism ; RNA-Binding Proteins / physiology ; Saccharomyces cerevisiae / metabolism ; Saccharomyces cerevisiae / physiology ; Saccharomyces cerevisiae Proteins / metabolism ; Saccharomyces cerevisiae Proteins / physiology ; Spores, Fungal / enzymology References: J Biol Chem. 2008 Nov 14;283(46):31706-18. (PMID: 18775984) ; Cell. 1999 Apr 30;97(3):313-24. (PMID: 10319812) ; RNA. 2006 Jul;12(7):1361-72. (PMID: 16738408) ; Nucleic Acids Res. 2009 Jul;37(12):3865-77. (PMID: 19386620) ; Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14787-92. (PMID: 20679221) ; EMBO J. 1995 Aug 15;14(16):4001-9. (PMID: 7664739) ; RNA. 2010 Jan;16(1):211-20. (PMID: 19926722) ; Nucleic Acids Res. 2003 Jul 1;31(13):3406-15. (PMID: 12824337) ; Nucleic Acids Res. 2007;35(5):1411-20. (PMID: 17284461) ; J Biol Chem. 2005 Sep 16;280(37):32101-6. (PMID: 16046409) ; Mol Cell. 2000 Aug;6(2):329-38. (PMID: 10983980) ; Mol Cell. 2008 Dec 5;32(5):735-46. (PMID: 19061648) ; Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14548-53. (PMID: 11114178) ; Nucleic Acids Res. 2008 May;36(8):2787-98. (PMID: 18375978) ; RNA. 1998 Apr;4(4):374-93. (PMID: 9630245) ; Nucleic Acids Res. 2000 Apr 15;28(8):1700-6. (PMID: 10734188) ; Nucleic Acids Res. 2011 Apr;39(8):3427-45. (PMID: 21208980) ; Mol Cell. 2000 Nov;6(5):1089-98. (PMID: 11106748) ; Curr Biol. 2001 Jul 10;11(13):1001-9. (PMID: 11470404) ; Genes Dev. 2010 Dec 1;24(23):2693-704. (PMID: 21123654) ; J Biol Chem. 2005 Feb 11;280(6):4021-4. (PMID: 15590684) ; Trends Biochem Sci. 2010 Mar;35(3):169-78. (PMID: 19959365) ; Genetics. 1997 Jul;146(3):817-34. (PMID: 9215889) ; Genes Dev. 1994 Apr 1;8(7):843-54. (PMID: 7926772) ; Cell. 1991 Sep 20;66(6):1257-68. (PMID: 1840507) ; J Biol Chem. 2005 Apr 1;280(13):12397-404. (PMID: 15684427) ; Genetics. 2003 Jan;163(1):47-54. (PMID: 12586695) ; Mol Cell Biol. 1992 Apr;12(4):1460-8. (PMID: 1532228) ; Mol Gen Genet. 1997 Jul;255(4):410-9. (PMID: 9267437) ; RNA. 2008 Aug;14(8):1617-31. (PMID: 18596255) ; Mol Cell Biol. 1990 May;10(5):2379-89. (PMID: 2183032) ; Mol Cell Biol. 2000 Sep;20(17):6287-99. (PMID: 10938105) ; Mol Cell. 2002 Apr;9(4):891-901. (PMID: 11983179) ; RNA. 1999 Feb;5(2):221-34. (PMID: 10024174) ; Mol Biol Cell. 2006 Jul;17(7):3221-31. (PMID: 16687569) ; Genes Cells. 1997 Jan;2(1):65-79. (PMID: 9112441) ; EMBO J. 1998 Oct 1;17(19):5783-95. (PMID: 9755178) ; EMBO J. 1995 Aug 15;14(16):4010-21. (PMID: 7664740) ; Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1522-7. (PMID: 17244705) ; Yeast. 2002 Jan 15;19(1):43-54. (PMID: 11754482) ; Genes Dev. 1999 Mar 1;13(5):569-80. (PMID: 10072385) ; Nucleic Acids Res. 1996 Dec 1;24(23):4614-23. (PMID: 8972845) ; Cell. 1993 Apr 23;73(2):407-15. (PMID: 8477451) ; Nat Genet. 2000 Dec;26(4):415-23. (PMID: 11101837) ; Mol Cell Biol. 1999 Dec;19(12):7933-43. (PMID: 10567519) ; RNA. 2004 Dec;10(12):1925-33. (PMID: 15525712) ; RNA. 2010 May;16(5):1018-31. (PMID: 20360394) ; Annu Rev Biochem. 1982;51:617-54. (PMID: 6180681) ; RNA. 1999 Jun;5(6):819-31. (PMID: 10376880) ; Mol Cell Biol. 1995 Apr;15(4):1953-60. (PMID: 7891689) ; Nucleic Acids Res. 2004 Feb 18;32(3):1242-50. (PMID: 14973223) Grant Information: GM50288 United States GM NIGMS NIH HHS; GM52470 United States GM NIGMS NIH HHS Substance Nomenclature: 0 (MER1 protein, S cerevisiae) ; 0 (Nuclear Proteins) ; 0 (Pch2 protein, S cerevisiae) ; 0 (RNA Precursors) ; 0 (RNA, Messenger) ; 0 (RNA-Binding Proteins) ; 0 (SAE2 protein, S cerevisiae) ; 0 (Saccharomyces cerevisiae Proteins) ; 12133JR80S (Guanosine) ; 40027-70-1 (N(2),N(2),7-trimethylguanosine) ; EC 2.1.1.- (Methyltransferases) ; EC 2.1.1.- (trimethylguanosine synthase) ; EC 3.1.- (Endonucleases) Entry Date(s): Date Created: 20110315 Date Completed: 20111003 Latest Revision: 20211020 Update Code: 20231215 PubMed Central ID: PMC3141232

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An essential role for trimethylguanosine RNA caps in Saccharomyces cerevisiae meiosis and their requirement for splicing of SAE3 and PCH2 meiotic pre-mRNAs.