Divergence of a conserved elongation factor and transcription regulation in budding and fission yeast

被引:59
作者
Booth, Gregory T. [1 ]
Wang, Isabel X. [2 ]
Cheung, Vivian G. [2 ]
Lis, John T. [1 ]
机构
[1] Cornell Univ, Dept Mol Biol & Genet, Ithaca, NY 14853 USA
[2] Univ Michigan, Inst Life Sci, Ann Arbor, MI 48109 USA
基金
美国国家卫生研究院;
关键词
RNA-POLYMERASE-II; GENOME-WIDE ANALYSIS; SCHIZOSACCHAROMYCES-POMBE; SACCHAROMYCES-CEREVISIAE; BIDIRECTIONAL PROMOTERS; GENE-REGULATION; TERMINATION; INITIATION; MECHANISMS; BINDING;
D O I
10.1101/gr.204578.116
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Complex regulation of gene expression in mammals has evolved from simpler eukaryotic systems, yet the mechanistic features of this evolution remain elusive. Here, we compared the transcriptional landscapes of the distantly related budding and fission yeast. We adapted the Precision Run-On sequencing (PRO-seq) approach to map the positions of RNA polymerase active sites genome-wide in Schizosaccharomyces pombe and Saccharomyces cerevisiae. Additionally, we mapped preferred sites of transcription initiation in each organism using PRO-cap. Unexpectedly, we identify a pause in early elongation, specific to S. pombe, that requires the conserved elongation factor subunit Spt4 and resembles promoter-proximal pausing in metazoans. PRO-seq profiles in strains lacking Spt4 reveal globally elevated levels of transcribing RNA Polymerase II (Pol II) within genes in both species. Messenger RNA abundance, however, does not reflect the increases in Pol II density, indicating a global reduction in elongation rate. Together, our results provide the first base-pair resolution map of transcription elongation in S. pombe and identify divergent roles for Spt4 in controlling elongation in budding and fission yeast.
引用
收藏
页码:799 / 811
页数:13
相关论文
共 78 条
[11]   Signaling Pathways Differentially Affect RNA Polymerase II Initiation, Pausing, and Elongation Rate in Cells [J].
Danko, Charles G. ;
Hah, Nasun ;
Luo, Xin ;
Martins, Andre L. ;
Core, Leighton ;
Lis, John T. ;
Siepel, Adam ;
Kraus, W. Lee .
MOLECULAR CELL, 2013, 50 (02) :212-222
[12]   Spt6 Regulates Intragenic and Antisense Transcription, Nucleosome Positioning, and Histone Modifications Genome-Wide in Fission Yeast [J].
DeGennaro, Christine M. ;
Alver, Burak H. ;
Marguerat, Samuel ;
Stepanova, Ekaterina ;
Davis, Christopher P. ;
Baehler, Juerg ;
Park, Peter J. ;
Winston, Fred .
MOLECULAR AND CELLULAR BIOLOGY, 2013, 33 (24) :4779-4792
[13]   STAR: ultrafast universal RNA-seq aligner [J].
Dobin, Alexander ;
Davis, Carrie A. ;
Schlesinger, Felix ;
Drenkow, Jorg ;
Zaleski, Chris ;
Jha, Sonali ;
Batut, Philippe ;
Chaisson, Mark ;
Gingeras, Thomas R. .
BIOINFORMATICS, 2013, 29 (01) :15-21
[14]   Yeast evolutionary genomics [J].
Dujon, Bernard .
NATURE REVIEWS GENETICS, 2010, 11 (07) :512-524
[15]   Determinants of RNA metabolism in the Schizosaccharomyces pombe genome [J].
Eser, Philipp ;
Wachutka, Leonhard ;
Maier, Kerstin C. ;
Demel, Carina ;
Boroni, Mariana ;
Iyer, Srignanakshi ;
Cramer, Patrick ;
Gagneur, Julien .
MOLECULAR SYSTEMS BIOLOGY, 2016, 12 (02)
[16]   Effects of Transcription Elongation Rate and Xrn2 Exonuclease Activity on RNA Polymerase II Termination Suggest Widespread Kinetic Competition [J].
Fong, Nova ;
Brannan, Kristopher ;
Erickson, Benjamin ;
Kim, Hyunmin ;
Cortazar, Michael A. ;
Sheridan, Ryan M. ;
Nguyen, Tram ;
Karp, Shai ;
Bentley, David L. .
MOLECULAR CELL, 2015, 60 (02) :256-267
[17]   Defining mechanisms that regulate RNA polymerase II transcription in vivo [J].
Fuda, Nicholas J. ;
Ardehali, M. Behfar ;
Lis, John T. .
NATURE, 2009, 461 (7261) :186-192
[18]   Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms [J].
García-Martínez, J ;
Aranda, A ;
Pérez-Ortín, JE .
MOLECULAR CELL, 2004, 15 (02) :303-313
[19]   Regulating the regulators: the pervasive effects of Pol II pausing on stimulus-responsive gene networks [J].
Gilchrist, Daniel A. ;
Fromm, George ;
dos Santos, Gilberto ;
Pham, Linh N. ;
McDaniel, Ivy E. ;
Burkholder, Adam ;
Fargo, David C. ;
Adelman, Karen .
GENES & DEVELOPMENT, 2012, 26 (09) :933-944
[20]   Chromatin architectures at fission yeast transcriptional promoters and replication origins [J].
Givens, Robert M. ;
Lai, William K. M. ;
Rizzo, Jason M. ;
Bard, Jonathan E. ;
Mieczkowski, Piotr A. ;
Leatherwood, Janet ;
Huberman, Joel A. ;
Buck, Michael J. .
NUCLEIC ACIDS RESEARCH, 2012, 40 (15) :7176-7189