Current Genetics

, Volume 62, Issue 2, pp 317–319 | Cite as

Understanding the regulation of coding and noncoding transcription in cell populations

Review

Abstract

Whole transcriptome analyses have unveiled the uncomfortable truth that we know less about how transcription is regulated then we thought. In addition to its role in classic promoter-driven transcription of coding RNA, it is now clear that RNA Pol II also drives abundant expression of noncoding RNA. For the majority of this the functional significance remains unclear. Moreover, its regulation and impact are hard to predict because it often proceeds in unexpected ways from cryptic promoters, including by driving convergent antisense transcription from within 3′ UTRs. This review suggests that its time to rethink how we envisage gene expression by inclusion of the regulatory architecture of the full genetic locus, and expanding our thinking to encompass the fact that we generally study cells within heterogeneous populations.

Keywords

Gene expression RNA metabolism 3′-End formation Noncoding RNA Convergent antisense transcription 

References

  1. Alcid EA, Tsukiyama T (2014) ATP-dependent chromatin remodeling shapes the long noncoding RNA landscape. Genes Dev 28:2348–2360CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aragon AD, Rodriguez AL, Meirelles O, Roy S, Davidson GS, Tapia PH, Allen C, Joe R, Benn D, Werner-Washburne M (2008) Characterization of differentiated quiescent and non-quiescent cells in yeast stationary-phase cultures. Mol Biol Cell 19:1271–1280CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ben-Shitrit T, Yosef N, Shemesh K, Sharan R, Ruppin E, Kupiec M (2012) Systematic identification of gene annotation errors in the widely used yeast mutation collections. Nat Methods 9:373–378CrossRefPubMedGoogle Scholar
  4. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proc Natl Acad Sci USA 106:18321–18326CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cap M, Stepanek L, Harant K, Vachova L, Palkova Z (2012) Cell differentiation within a yeast colony: metabolic and regulatory parallels with a tumor-affected organism. Mol Cell 46:436–448CrossRefPubMedGoogle Scholar
  6. Garcia JF, Parker R (2015) MS2 coat proteins bound to yeast mRNAs block 5′ to 3′ degradation and trap mRNA decay products: implications for the localization of mRNAs by MS2-MCP system. RNA 21:1393–1395CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425:737–741CrossRefPubMedGoogle Scholar
  8. Granovskaia MV, Jensen LJ, Ritchie ME, Toedling J, Ning Y, Bork P, Huber W, Steinmetz LM (2010) High-resolution transcription atlas of the mitotic cell cycle in budding yeast. Genome Biol 11:R24CrossRefPubMedPubMedCentralGoogle Scholar
  9. Grzechnik P, Tan-Wong SM, Proudfoot NJ (2014) Terminate and make a loop: regulation of transcriptional directionality. Trends Biochem Sci 39:319–327CrossRefPubMedPubMedCentralGoogle Scholar
  10. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O’Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425:686–691CrossRefPubMedGoogle Scholar
  11. Neil H, Malabat C, d’Aubenton-Carafa Y, Xu Z, Steinmetz LM, Jacquier A (2009) Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457:1038–1042CrossRefPubMedGoogle Scholar
  12. Pena-Castillo L, Hughes TR (2007) Why are there still over 1000 uncharacterized yeast genes? Genetics 176:7–14CrossRefPubMedPubMedCentralGoogle Scholar
  13. Prescott EM, Proudfoot NJ (2002) Transcriptional collision between convergent genes in budding yeast. Proc Natl Acad Sci USA 99:8796–8801CrossRefPubMedPubMedCentralGoogle Scholar
  14. Swaminathan A, Beilharz TH (2015) Epitope-tagged yeast strains reveal promoter driven changes to 3′-end formation and convergent antisense-transcription from common 3′ UTRs. Nucleic Acids Res. http://www.ncbi.nlm.nih.gov/pubmed/26481348
  15. Tan-Wong SM, Zaugg JB, Camblong J, Xu Z, Zhang DW, Mischo HE, Ansari AZ, Luscombe NM, Steinmetz LM, Proudfoot NJ (2012) Gene loops enhance transcriptional directionality. Science 338:671–675CrossRefPubMedPubMedCentralGoogle Scholar
  16. Traven A, Janicke A, Harrison P, Swaminathan A, Seemann T, Beilharz TH (2012) Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities. PLoS One 7:e46243CrossRefPubMedPubMedCentralGoogle Scholar
  17. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM (2009) Bidirectional promoters generate pervasive transcription in yeast. Nature 457:1033–1037CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Development and Stem Cells Program, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery InstituteMonash UniversityMelbourneAustralia

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