Intragenic transcription of a noncoding RNA modulates expression of ASP3 in budding yeast.
Inter- and intragenic noncoding transcription is widespread in eukaryotic genomes; however, the purpose of these types of transcription is still poorly understood. Here, we show that intragenic sense-oriented transcription within the budding yeast ASP3 coding region regulates a constitutively and immediately accessible promoter for the transcription of full-length ASP3. Expression of this short intragenic transcript is independent of GATA transcription factors, which are essential for the activation of full-length ASP3, and independent of RNA polymerase II (RNAPII). Furthermore, we found that an intragenic control element is required for the expression of this noncoding RNA (ncRNA). Continuous expression of the short ncRNA maintains a high level of trimethylation of histone H3 at lysine 4 (H3K4me3) at the ASP3 promoter and makes this region more accessible for RNAPII to transcribe the full-length ASP3. Our results show for the first time that intragenic noncoding transcription promotes gene expression.
Huang
Yu-Ching
YC
Department of Microbiology, College of Medicine, National Taiwan University, Taipei 10051, Taiwan.
Chen
Hung-Ta
HT
Teng
Shu-Chun
SC
D042002:Chromatin Assembly and Disassembly; D050980:GATA Transcription Factors / Q000235:genetics / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D016366:Open Reading Frames; D011401:Promoter Regions, Genetic; D012319:RNA Polymerase II / Q000235:genetics / Q000378:metabolism; D022661:RNA, Untranslated / Q000235:genetics*; D012441:Saccharomyces cerevisiae / Q000235:genetics* / Q000378:metabolism*; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D014158:Transcription, Genetic
C096100:GAT1 protein, S cerevisiae; D050980:GATA Transcription Factors; C071664:GLN3 protein, S cerevisiae; D022661:RNA, Untranslated; D029701:Saccharomyces cerevisiae Proteins; D014157:Transcription Factors; D012319:RNA Polymerase II
Nat Cell Biol. 2008 Feb;10(2):228-36
18157120
EMBO J. 2006 Dec 13;25(24):5726-34
17139254
J Biol Chem. 2000 Nov 17;275(46):35727-33
10940301
Cell. 2007 Jun 29;129(7):1311-23
17604720
Trends Genet. 2003 Nov;19(11):629-39
14585615
Mol Cell. 2003 Nov;12(5):1325-32
14636589
EMBO J. 2009 Jun 17;28(12):1679-80
19532144
Appl Biochem Biotechnol. 1999 Spring;77-79:311-6
10399275
Mol Cell Biol. 1987 May;7(5):1602-11
3299050
Mol Cell Biol. 1986 Jun;6(6):2089-97
3537713
Cold Spring Harb Perspect Biol. 2009 Oct;1(4):a000224
20066094
Science. 2008 Dec 12;322(5908):1717-20
18988810
FEMS Yeast Res. 2006 Aug;6(5):777-91
16879428
Genes Dev. 2009 Jul 1;23(13):1534-45
19571181
Nucleic Acids Res. 1987 Oct 26;15(20):8125-48
3313277
PLoS Biol. 2008 Dec 23;6(12):2817-30
19108609
EMBO J. 2007 Dec 12;26(24):4996-5006
18007593
J Biol Chem. 1978 Feb 25;253(4):1297-304
342521
Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9450-4
7568152
J Biol Chem. 2003 Jul 18;278(29):26303-6
12764140
Methods Mol Biol. 2006;313:225-44
16118437
Mol Cell Biol. 2006 Nov;26(21):7901-12
16940175
Yeast. 2003 Jan 15;20(1):31-7
12489124
Mol Cell. 2003 Mar;11(3):709-19
12667453
Genes Dev. 2003 Feb 15;17(4):529-40
12600945
Curr Opin Genet Dev. 2003 Apr;13(2):154-60
12672492
Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14866-70
10611304
Mol Cell. 2008 Oct 24;32(2):232-46
18951091
Nature. 2009 Feb 19;457(7232):1038-42
19169244
Genes Dev. 2008 Mar 1;22(5):615-26
18316478
Nature. 1999 Dec 9;402(6762):689-92
10604478
Nature. 2007 Feb 8;445(7128):666-70
17237763
Yeast. 1999 Jul;15(10B):963-72
10407276
J Bacteriol. 1980 Jul;143(1):422-6
6995441
J Biol Chem. 1988 Aug 25;263(24):11948-53
3042786
J Bacteriol. 1988 Feb;170(2):708-13
2892826
Genome Biol. 2005;6(13):R111
16420678
Nat Biotechnol. 2003 Apr;21(4):379-86
12640466
Nature. 2008 Jul 3;454(7200):126-30
18509338
Mol Cell. 2008 Nov 21;32(4):465-77
19026778
Cell. 2007 Nov 16;131(4):706-17
18022365
Nature. 2000 Jan 6;403(6765):41-5
10638745
Science. 2002 May 3;296(5569):916-9
11988577
Proc Natl Acad Sci U S A. 1981 Apr;78(4):2199-203
6264467
Science. 2007 Nov 2;318(5851):798-801
17916692
Genes Dev. 1999 Dec 15;13(24):3271-9
10617575
Proc Natl Acad Sci U S A. 2007 May 8;104(19):8011-6
17470801
Science. 2005 May 20;308(5725):1149-54
15790807
Mol Cell. 2008 Dec 5;32(5):685-95
19061643
Nature. 2004 Jun 3;429(6991):571-4
15175754
Genes Dev. 2000 Oct 1;14(19):2452-60
11018013
Cell. 2006 Nov 17;127(4):735-45
17110333
Nature. 2002 Sep 26;419(6905):407-11
12353038
Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3262-7
16484372
J Exp Med. 2001 Jun 18;193(12):1351-9
11413190
Mol Cell Biol. 1984 Dec;4(12):2758-66
6152012