Skip to main content
Log in

Understanding the regulation of coding and noncoding transcription in cell populations

  • Review
  • Published:
Current Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Alcid EA, Tsukiyama T (2014) ATP-dependent chromatin remodeling shapes the long noncoding RNA landscape. Genes Dev 28:2348–2360

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 19:1271–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:373–378

    Article  CAS  PubMed  Google Scholar 

  • 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 106:18321–18326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 46:436–448

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1393–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 425:737–741

    Article  CAS  PubMed  Google Scholar 

  • 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:R24

    Article  PubMed  PubMed Central  Google Scholar 

  • Grzechnik P, Tan-Wong SM, Proudfoot NJ (2014) Terminate and make a loop: regulation of transcriptional directionality. Trends Biochem Sci 39:319–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 425:686–691

    Article  CAS  PubMed  Google Scholar 

  • 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 457:1038–1042

    Article  CAS  PubMed  Google Scholar 

  • Pena-Castillo L, Hughes TR (2007) Why are there still over 1000 uncharacterized yeast genes? Genetics 176:7–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prescott EM, Proudfoot NJ (2002) Transcriptional collision between convergent genes in budding yeast. Proc Natl Acad Sci USA 99:8796–8801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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 338:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e46243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 457:1033–1037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Traude Helene Beilharz.

Additional information

Communicated by M. Kupiec.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beilharz, T.H. Understanding the regulation of coding and noncoding transcription in cell populations. Curr Genet 62, 317–319 (2016). https://doi.org/10.1007/s00294-015-0547-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0547-1

Keywords

Navigation