Skip to main content

Functions of Long Non-Coding RNAs in Non-mammalian Systems

  • Chapter
  • First Online:
Book cover Molecular Biology of Long Non-coding RNAs
  • 1667 Accesses

Abstract

Transcription of eukaryotic genomes is pervasive, with most if not all bases transcribed. A single stretch of genomic sequence is commonly represented in numerous distinct transcripts, due to the use of alternative transcription start and termination sites, the ability of RNA polymerase II (Pol II) to transcribe in either orientation or alternative RNA processing events. The transcriptome is thus overwhelmingly complex and contains many so-called long non-coding RNAs (lncRNAs), which lack protein coding capacity. These are distinct from classically annotated classes of structural RNAs (e.g. rRNA, tRNA, snRNA, snoRNA), or the more recently discovered small regulatory RNAs (siRNA, miRNA and piRNA). In this chapter, we focus on recent advances toward understanding the functions of lncRNAs in non-mammalian systems including yeast, plants and flies. The amenability of these organisms to genetic manipulation and their short generation time has enabled rapid progress to be made, often at the mechanistic level. In mammalian cells, there is extensive crosstalk between lncRNAs and small (~21–25 nt) regulatory RNAs. However, these very small RNAs are apparently absent from the yeast Saccharomyces cerevisiae, while lncRNAs and small regulatory RNAs in Arabidopsis are transcribed by distinct, specialized polymerases. Studies in these organisms have helped define the individual contributions of lncRNAs and small RNAs, and reveal how they collaborate and compete in RNA-dependent regulatory pathways.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alekseyenko, A. A., Peng, S., Larschan, E., Gorchakov, A. A., Lee, O. K., Kharchenko, P., et al. (2008). A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell, 134(4), 599–609.

    Article  PubMed  CAS  Google Scholar 

  • Arigo, J. T., Carroll, K. L., Ames, J. M., & Corden, J. L. (2006). Regulation of yeast NRD1 expression by premature transcription termination. Molecular Cell, 21(5), 641–651.

    Article  PubMed  CAS  Google Scholar 

  • Berretta, J., Pinskaya, M., & Morillon, A. (2008). A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in Saccharomyces cerevisiae. Genes & Development, 22(5), 615–626.

    Article  CAS  Google Scholar 

  • Bird, A. J., Gordon, M., Eide, D. J., & Winge, D. R. (2006). Repression of ADH1 and ADH3 during zinc deficiency by Zap1-induced intergenic RNA transcripts. EMBO Journal, 25(24), 5726–5734.

    Article  PubMed  CAS  Google Scholar 

  • Brar, G. A., Yassour, M., Friedman, N., Regev, A., Ingolia, N. T., & Weissman, J. S. (2012). High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science, 335(6068), 552–557.

    Article  PubMed  CAS  Google Scholar 

  • Buhler, M. (2009). RNA turnover and chromatin-dependent gene silencing. Chromosoma, 118(2), 141–151.

    Article  PubMed  CAS  Google Scholar 

  • Buhler, M., Verdel, A., & Moazed, D. (2006). Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell, 125(5), 873–886.

    Article  PubMed  CAS  Google Scholar 

  • Buhler, M., Spies, N., Bartel, D. P., & Moazed, D. (2008). TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nature Structural & Molecular Biology, 15(10), 1015–1023.

    Article  CAS  Google Scholar 

  • Bühler, M., Haas, W., Gygi, S. P., & Moazed, D. (2007). RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell, 129(4), 707–721.

    Article  PubMed  CAS  Google Scholar 

  • Bumgarner, S. L., Dowell, R. D., Grisafi, P., Gifford, D. K., & Fink, G. R. (2009). Toggle involving cis-interfering non-coding RNAs controls variegated gene expression in yeast. Proceedings of the National Academy of Sciences of the United States of America, 106(43), 18321–18326.

    Article  PubMed  CAS  Google Scholar 

  • Bumgarner, S. L., Neuert, G., Voight, F. R., Symbor-Nagrabska, A., Grisafi, P., van Oudenaarden, A., et al. (2012). Single-cell analysis reveals that non-coding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment. Molecular Cell, 45, 1–13.

    Article  CAS  Google Scholar 

  • Camblong, J., Iglesias, N., Fickentscher, C., Dieppois, G., & Stutz, F. (2007). Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in Saccharomyces cerevisiae. Cell, 131(4), 706–717.

    Article  PubMed  CAS  Google Scholar 

  • Camblong, J., Beyrouthy, N., Guffanti, E., Schlaepfer, G., Steinmetz, L. M., & Stutz, F. (2009). Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes & Development, 23(13), 1534–1545.

    Article  CAS  Google Scholar 

  • Cernilogar, F. M., Onorati, M. C., Kothe, G. O., Burroughs, A. M., Parsi, K. M., Breiling, A., et al. (2011). Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature, 480(7377), 391–395.

    Article  PubMed  CAS  Google Scholar 

  • Cheung, V., Chua, G., Batada, N. N., Landry, C. R., Michnick, S. W., Hughes, T. R., et al. (2008). Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biology, 6(11), e277.

    Article  PubMed  CAS  Google Scholar 

  • Chu, C., Qu, K., Zhong Franklin, L., Artandi Steven, E., & Chang Howard, Y. (2011). Genomic maps of long non-coding RNA occupancy reveal principles of RNA-chromatin interactions. Molecular Cell, 44(4), 667–678.

    Article  PubMed  CAS  Google Scholar 

  • Churchman, L. S., & Weissman, J. S. (2011). Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature, 469(7330), 368–373.

    Article  PubMed  CAS  Google Scholar 

  • Conrad, T., Cavalli, F. M. G., Vaquerizas, J. M., Luscombe, N. M., & Akhtar, A. (2012). Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters. Science, 337(6095), 742–746.

    Article  PubMed  CAS  Google Scholar 

  • Creamer, T. J., Darby, M. M., Jamonnak, N., Schaughency, P., Hao, H., Wheelan, S. J., et al. (2011). Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae non-poly(A) termination pathway: Nrd1, Nab3, and Sen1. PLoS Genetics, 7(10), e1002329.

    Article  PubMed  CAS  Google Scholar 

  • Czech, B., & Hannon, G. J. (2011). Small RNA sorting: matchmaking for Argonautes. Nature Reviews Genetics, 12(1), 19–31.

    Article  PubMed  CAS  Google Scholar 

  • Czech, B., Malone, C. D., Zhou, R., Stark, A., Schlingeheyde, C., Dus, M., et al. (2008). An endogenous small interfering RNA pathway in Drosophila. Nature, 453(7196), 798–802.

    Article  PubMed  CAS  Google Scholar 

  • David, L., Huber, W., Granovskaia, M., Toedling, J., Palm, C. J., Bofkin, L., et al. (2006). A high-resolution map of transcription in the yeast genome. Proceedings of the National Academy of Sciences of the United States of America, 103(14), 5320–5325.

    Article  PubMed  CAS  Google Scholar 

  • Ding, D.-Q., Okamasa, K., Yamane, M., Tsutsumi, C., Haraguchi, T., Yamamoto, M., et al. (2012). Meiosis-specific non-coding RNA mediates robust pairing of homologous chromosomes in meiosis. Science, 336(6082), 732–736.

    Article  PubMed  CAS  Google Scholar 

  • El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., et al. (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes & Development, 21(20), 2539–2544.

    Article  CAS  Google Scholar 

  • Enderle, D., Beisel, C., Stadler, M. B., Gerstung, M., Athri, P., & Paro, R. (2011). Polycomb preferentially targets stalled promoters of coding and non-coding transcripts. Genome Research, 21(2), 216–226.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Martinez, J., Ayala, G., Pelechano, V., Chavez, S., Herrero, E., & Perez-Ortin, J. E. (2012). The relative importance of transcription rate, cryptic transcription and mRNA stability on shaping stress responses in yeast. Transcription, 3(1), 39–44.

    Article  PubMed  Google Scholar 

  • Geisler, S., Lojek, L., Khalil, A. M., Baker, K. E., & Coller, J. (2012). Decapping of long non-coding RNAs regulates inducible genes. Molecular Cell, 45(3), 279–291.

    Article  PubMed  CAS  Google Scholar 

  • Gelfand, B., Mead, J., Bruning, A., Apostolopoulos, N., Tadigotla, V., Nagaraj, V., et al. (2011). Regulated antisense transcription controls expression of cell-type-specific genes in yeast. Molecular and Cellular Biology, 31(8), 1701–1709.

    Article  PubMed  CAS  Google Scholar 

  • Ghildiyal, M., Seitz, H., Horwich, M. D., Li, C., Du, T., Lee, S., et al. (2008). Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science, 320(5879), 1077–1081.

    Article  PubMed  CAS  Google Scholar 

  • Granovskaia, M., Jensen, L., Ritchie, M., Toedling, J., Ning, Y., Bork, P., et al. (2010). High-resolution transcription atlas of the mitotic cell cycle in budding yeast. Genome Biology, 11(3), R24.

    Article  PubMed  CAS  Google Scholar 

  • Gudipati, R. K., Xu, Z., Lebreton, A., Seraphin, B., Steinmetz, L. M., Jacquier, A., et al. (2012). Extensive degradation of RNA precursors by the exosome in wild-type cells. Molecular Cell, 48(3), 409–421.

    Article  PubMed  CAS  Google Scholar 

  • Gupta, R. A., Shah, N., Wang, K. C., Kim, J., Horlings, H. M., Wong, D. J., et al. (2010). Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature, 464(7291), 1071–1076.

    Article  PubMed  CAS  Google Scholar 

  • Haag, J. R., Ream, T. S., Marasco, M., Nicora, C. D., Norbeck, A. D., Pasa-Tolic, L., Pikaard, C. S. (2012). In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Molecular Cell, 48, 811–818.

    Google Scholar 

  • Hainer, S. J., & Martens, J. A. (2011). Identification of histone mutants that are defective for transcription-coupled nucleosome occupancy. Molecular and Cellular Biology, 31(17), 3557–3568.

    Article  PubMed  CAS  Google Scholar 

  • Hainer, S. J., Pruneski, J. A., Mitchell, R. D., Monteverde, R. M., & Martens, J. A. (2011). Intergenic transcription causes repression by directing nucleosome assembly. Genes & Development, 25(1), 29–40.

    Article  CAS  Google Scholar 

  • Halic, M., & Moazed, D. (2010). Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell, 140(4), 504–516.

    Article  PubMed  CAS  Google Scholar 

  • Halme, A., Bumgarner, S., Styles, C., & Fink, G. R. (2004). Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell, 116(3), 405–415.

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa, Y., Brockdorff, N., Kawano, S., Tsutui, K., Tsutui, K., & Nakagawa, S. (2010). The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Developmental Cell, 19(3), 469–476.

    Article  PubMed  CAS  Google Scholar 

  • Hazen, S., Naef, F., Quisel, T., Gendron, J., Chen, H., Ecker, J., et al. (2009). Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biology, 10(2), R17.

    Article  PubMed  CAS  Google Scholar 

  • He, X.-J., Hsu, Y.-F., Zhu, S., Wierzbicki, A. T., Pontes, O., Pikaard, C. S., et al. (2009). An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell, 137(3), 498–508.

    Article  PubMed  CAS  Google Scholar 

  • Heo, J. B., & Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic non-coding RNA. Science, 331(6013), 76–79.

    Article  PubMed  CAS  Google Scholar 

  • Herr, A. J., Jensen, M. B., Dalmay, T., & Baulcombe, D. C. (2005). RNA polymerase IV directs silencing of endogenous DNA. Science, 308(5718), 118–120.

    Article  PubMed  CAS  Google Scholar 

  • Hessle, V., von Euler, A., González de Valdivia, E., & Visa, N. (2012). Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore. RNA, 18(8), 1466–1474.

    Article  PubMed  CAS  Google Scholar 

  • Hirota, K., Miyoshi, T., Kugou, K., Hoffman, C. S., Shibata, T., & Ohta, K. (2008). Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature, 456(7218), 130–134.

    Article  PubMed  CAS  Google Scholar 

  • Hobson, D. J., Wei, W., Steinmetz, L. M., & Svejstrup, J. Q. (2012). RNA polymerase II collision interrupts convergent transcription. Molecular Cell, 48(3), 365–374.

    Article  PubMed  CAS  Google Scholar 

  • Hongay, C. F., Grisafi, P. L., Galitski, T., & Fink, G. R. (2006). Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell, 127(4), 735–745.

    Article  PubMed  CAS  Google Scholar 

  • Houseley, J., & Tollervey, D. (2008). The nuclear RNA surveillance machinery: The link between ncRNAs and genome structure in budding yeast? Biochimica et Biophysica Acta (BBA): Gene Regulatory Mechanisms, 1779(4), 239–246.

    Article  CAS  Google Scholar 

  • Houseley, J., & Tollervey, D. (2011). Repeat expansion in the budding yeast ribosomal DNA can occur independently of the canonical homologous recombination machinery. Nucleic Acids Research, 39(20), 8778–8791.

    Article  PubMed  CAS  Google Scholar 

  • Houseley, J., Kotovic, K., El Hage, A., & Tollervey, D. (2007). Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO Journal, 26(24), 4996–5006.

    Article  PubMed  CAS  Google Scholar 

  • Houseley, J., Rubbi, L., Grunstein, M., Tollervey, D., & Vogelauer, M. (2008). A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Molecular Cell, 32(5), 685–695.

    Article  PubMed  CAS  Google Scholar 

  • Huettel, B., Kanno, T., Daxinger, L., Aufsatz, W., Matzke, A. J., & Matzke, M. (2006). Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO Journal, 25(12), 2828–2836.

    Article  PubMed  CAS  Google Scholar 

  • Jenks, M. H., O’Rourke, T. W., & Reines, D. (2008). Properties of an intergenic terminator and start site switch that regulate IMD2 transcription in yeast. Molecular and Cellular Biology, 28(12), 3883–3893.

    Article  PubMed  CAS  Google Scholar 

  • Jeon, Y., & Lee Jeannie, T. (2011). YY1 tethers Xist RNA to the inactive X nucleation center. Cell, 146(1), 119–133.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, T. K., Carrington, L. B., Hallas, R. J., & McKechnie, S. W. (2009). Protein synthesis rates in Drosophila associate with levels of the hsr-omega nuclear transcript. Cell Stress Chaperones, 14(6), 569–577.

    Article  PubMed  CAS  Google Scholar 

  • Kanhere, A., Viiri, K., Araújo, C. C., Rasaiyaah, J., Bouwman, R. D., Whyte, W. A., et al. (2010). Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Molecular Cell, 38(5), 675–688.

    Article  PubMed  CAS  Google Scholar 

  • Kanno, T., Huettel, B., Mette, M. F., Aufsatz, W., Jaligot, E., Daxinger, L., et al. (2005). Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nature Genetics, 37(7), 761–765.

    Article  PubMed  CAS  Google Scholar 

  • Kato, H., Goto, D. B., Martienssen, R. A., Urano, T., Furukawa, K., & Murakami, Y. (2005). RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science, 309(5733), 467–469.

    Article  PubMed  CAS  Google Scholar 

  • Kawamura, Y., Saito, K., Kin, T., Ono, Y., Asai, K., Sunohara, T., et al. (2008). Drosophila endogenous small RNAs bind to Argonaute-2 in somatic cells. Nature, 453(7196), 793–797.

    Article  PubMed  CAS  Google Scholar 

  • Kim, T., & Buratowski, S. (2009). Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5′ transcribed regions. Cell, 137(2), 259–272.

    Article  PubMed  CAS  Google Scholar 

  • Kim, K.-Y., & Levin, D. (2011). Mpk1 MAPK association with the Paf1 complex blocks Sen1-mediated premature transcription termination. Cell, 144(5), 745–756.

    Article  PubMed  CAS  Google Scholar 

  • Kim, H., Erickson, B., Luo, W., Seward, D., Graber, J. H., Pollock, D. D., et al. (2010). Gene-specific RNA polymerase II phosphorylation and the CTD code. Nature Structural & Molecular Biology, 17(10), 1279–1286.

    Article  CAS  Google Scholar 

  • Kim, T. S., Liu, C. L., Yassour, M., Holik, J., Friedman, N., Buratowski, S., et al. (2011). RNA polymerase mapping during stress responses reveals widespread nonproductive transcription in yeast. Genome Biology, 11(7), R75.

    Article  CAS  Google Scholar 

  • Kim, T., Xu, Z., Clauder-Münster, S., Steinmetz Lars, M., & Buratowski, S. (2012). Set3 HDAC mediates effects of overlapping non-coding transcription on gene induction kinetics. Cell, 150(6), 1158–1169.

    Article  PubMed  CAS  Google Scholar 

  • Kizer, K. O., Phatnani, H. P., Shibata, Y., Hall, H., Greenleaf, A. L., & Strahl, B. D. (2005). A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Molecular and Cellular Biology, 25(8), 3305–3316.

    Article  PubMed  CAS  Google Scholar 

  • Kuehner, J. N., & Brow, D. A. (2008). Regulation of a eukaryotic gene by GTP-dependent start site selection and transcription attenuation. Molecular Cell, 31(2), 201–211.

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia, S. C., Mallik, M., Singh, A. K., & Ray, M. (2012). The large non-coding hsromega-n transcripts are essential for thermotolerance and remobilization of hnRNPs, HP1 and RNA polymerase II during recovery from heat shock in Drosophila. Chromosoma, 121(1), 49–70.

    Article  PubMed  CAS  Google Scholar 

  • Lardenois, A., Liu, Y., Walther, T., Chalmel, F., Evrard, B., Granovskaia, M., et al. (2011). Execution of the meiotic non-coding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proceedings of the National Academy of Sciences, 108(3), 1058–1063.

    Article  CAS  Google Scholar 

  • Larschan, E., Bishop, E. P., Kharchenko, P. V., Core, L. J., Lis, J. T., Park, P. J., et al. (2011). X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature, 471(7336), 115–118.

    Article  PubMed  CAS  Google Scholar 

  • Lee, T. F., Gurazada, S. G., Zhai, J., Li, S., Simon, S. A., Matzke, M. A., et al. (2012). RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics, 7(7), 781–795.

    Article  PubMed  CAS  Google Scholar 

  • Li, C. F., Pontes, O., El-Shami, M., Henderson, I. R., Bernatavichute, Y. V., Chan, S. W. L., et al. (2006). An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell, 126(1), 93–106.

    Article  PubMed  CAS  Google Scholar 

  • Li, B., Jackson, J., Simon, M. D., Fleharty, B., Gogol, M., Seidel, C., et al. (2009). Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. Journal of Biological Chemistry, 284(12), 7970–7976.

    Article  PubMed  CAS  Google Scholar 

  • Lin, M. F., Jungreis, I., & Kellis, M. (2011). PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics, 27(13), i275–i282.

    Article  PubMed  CAS  Google Scholar 

  • Liu, J., Jung, C., Xu, J., Wang, H., Deng, S., Bernad, L., Arenas-Huertero, C., Chua, N. H. (2012). Genome-wide analysis uncovers regulation of long intergenic non-coding RNAs in Arabidopsis. Plant Cell, 24, 4333-4345.

    Google Scholar 

  • Luke, B., Panza, A., Redon, S., Iglesias, N., Li, Z., & Lingner, J. (2008). The Rat1p 5′ to 3′ exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Molecular Cell, 32(4), 465–477.

    Article  PubMed  CAS  Google Scholar 

  • Martens, J. A., Laprade, L., & Winston, F. (2004). Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature, 429(6991), 571–574.

    Article  PubMed  CAS  Google Scholar 

  • Martens, J. A., Wu, P. Y., & Winston, F. (2005). Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes & Development, 19(22), 2695–2704.

    Article  CAS  Google Scholar 

  • Martianov, I., Ramadass, A., Serra Barros, A., Chow, N., & Akoulitchev, A. (2007). Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature, 445(7128), 666–670.

    Article  PubMed  CAS  Google Scholar 

  • Matsuda, E., & Garfinkel, D. J. (2009). Posttranslational interference of Ty1 retrotransposition by antisense RNAs. Proceedings of the National Academy of Sciences, 106(37), 15657–15662.

    Article  CAS  Google Scholar 

  • Meller, V. H., & Rattner, B. P. (2002). The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO Journal, 21(5), 1084–1091.

    Article  PubMed  CAS  Google Scholar 

  • Mosher, R. A., Schwach, F., Studholme, D., & Baulcombe, D. C. (2008). PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proceedings of the National Academy of Sciences of the United States of America, 105(8), 3145–3150.

    Article  PubMed  CAS  Google Scholar 

  • Motamedi, M. R., Verdel, A., Colmenares, S. U., Gerber, S. A., Gygi, S. P., & Moazed, D. (2004). Two RNAi complexes, RITS and RDRC, physically interact and localize to non-coding centromeric RNAs. Cell, 119(6), 789–802.

    Article  PubMed  CAS  Google Scholar 

  • Murray, S. C., Serra Barros, A., Brown, D. A., Dudek, P., Ayling, J., & Mellor, J. (2012). A pre-initiation complex at the 3′-end of genes drives antisense transcription independent of divergent sense transcription. Nucleic Acids Research, 40(6), 2432–2444.

    Article  PubMed  CAS  Google Scholar 

  • Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., et al. (2008). The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320(5881), 1344–1349.

    Article  PubMed  CAS  Google Scholar 

  • Nam, J. W., & Bartel, D. P. (2012). Long non-coding RNAs in C. elegans. Genome Research, 22, 2529–2540.

    Article  PubMed  CAS  Google Scholar 

  • Nechaev, S., Fargo, D. C., dos Santos, G., Liu, L., Gao, Y., & Adelman, K. (2010). Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science, 327(5963), 335–338.

    Article  PubMed  CAS  Google Scholar 

  • Neil, H., Malabat, C., d’Aubenton-Carafa, Y., Xu, Z., Steinmetz, L. M., & Jacquier, A. (2009). Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature, 457(7232), 1038–1042.

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa, M., Komai, T., Katou, Y., Shirahige, K., Ito, T., & Toh-e, A. (2008). Nutrient-regulated antisense and intragenic RNAs modulate a signal transduction pathway in yeast. PLoS Biology, 6(12), e326.

    Article  CAS  Google Scholar 

  • Octavio, L. M., Gedeon, K., & Maheshri, N. (2009). Epigenetic and conventional regulation is distributed among activators of FLO11 allowing tuning of population-level heterogeneity in its expression. PLoS Genetics, 5(10), e1000673.

    Article  PubMed  CAS  Google Scholar 

  • Okamura, K., Balla, S., Martin, R., Liu, N., & Lai, E. C. (2008a). Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nature Structural & Molecular Biology, 15(6), 581–590.

    Article  CAS  Google Scholar 

  • Okamura, K., Chung, W.-J., Ruby, J. G., Guo, H., Bartel, D. P., & Lai, E. C. (2008b). The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature, 453(7196), 803–806.

    Article  PubMed  CAS  Google Scholar 

  • Onodera, Y., Haag, J. R., Ream, T., Costa Nunes, P., Pontes, O., & Pikaard, C. S. (2005). Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120(5), 613–622.

    Article  PubMed  CAS  Google Scholar 

  • O’Sullivan, J. M., Tan-Wong, S. M., Morillon, A., Lee, B., Coles, J., Mellor, J., et al. (2004). Gene loops juxtapose promoters and terminators in yeast. Nature Genetics, 36(9), 1014–1018.

    Article  PubMed  CAS  Google Scholar 

  • Pauli, A., Valen, E., Lin, M. F., Garber, M., Vastenhouw, N. L., Levin, J. Z., et al. (2012). Systematic identification of long non-coding RNAs expressed during zebrafish embryogenesis. Genome Research, 22(3), 577–591.

    Article  PubMed  CAS  Google Scholar 

  • Petruk, S., Sedkov, Y., Riley, K. M., Hodgson, J., Schweisguth, F., Hirose, S., et al. (2006). Transcription of bxd non-coding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell, 127(6), 1209–1221.

    Article  PubMed  CAS  Google Scholar 

  • Petruk, S., Sedkov, Y., Brock, H. W., & Mazo, A. (2007). A model for initiation of mosaic HOX gene expression patterns by non-coding RNAs in early embryos. RNA Biology, 4(1), 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer, V., & Lingner, J. (2012). TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genetics, 8(6), e1002747.

    Article  PubMed  CAS  Google Scholar 

  • Pinskaya, M., Gourvennec, S., & Morillon, A. (2009). H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO Journal, 28, 1697–1707.

    Article  PubMed  CAS  Google Scholar 

  • Pontes, O., Li, C. F., Costa Nunes, P., Haag, J., Ream, T., Vitins, A., et al. (2006). The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell, 126(1), 79–92.

    Article  PubMed  CAS  Google Scholar 

  • Pontes, O., Costa-Nunes, P., Vithayathil, P., & Pikaard, C. S. (2009). RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Molecular Plant, 2(4), 700–710.

    Article  PubMed  CAS  Google Scholar 

  • Pontier, D., Yahubyan, G., Vega, D., Bulski, A., Saez-Vasquez, J., Hakimi, M. A., et al. (2005). Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes & Development, 19(17), 2030–2040.

    Article  CAS  Google Scholar 

  • Prasanth, K. V., Rajendra, T. K., Lal, A. K., & Lakhotia, S. C. (2000). Omega speckles—a novel class of nuclear speckles containing hnRNPs associated with non-coding hsr-omega RNA in Drosophila. Journal of Cell Science, 113(19), 3485–3497.

    PubMed  CAS  Google Scholar 

  • Purzycka, K. J., Legiewicz, M., Matsuda, E., Eizentstat, L. D., Lusvarghi, S., Saha, A., Le Grice, S. F. J., Garfinkel, D. J. (2012). Exploring Ty1 retrotransposon RNA structure within virus-like particles. Nucleic Acids Research, 41, 463-473.

    Google Scholar 

  • Redon, S., Reichenbach, P., & Lingner, J. (2010). The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Research, 38(17), 5797–5806.

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Turcu, F. E., Zhang, K., Zofall, M., Chen, E., & Grewal, S. I. (2011). Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nature Structural & Molecular Biology, 18(10), 1132–1138.

    Article  CAS  Google Scholar 

  • Rhee, H. S., & Pugh, B. F. (2012). Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature, 483(7389), 295–301.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Gil, A., Garcia-Martinez, J., Pelechano, V., Munoz-Centeno Mde, L., Geli, V., Perez-Ortin, J. E., et al. (2010). The distribution of active RNA polymerase II along the transcribed region is gene-specific and controlled by elongation factors. Nucleic Acids Research, 38(14), 4651–4664.

    Article  PubMed  CAS  Google Scholar 

  • Schmitz, K.-M., Mayer, C., Postepska, A., & Grummt, I. (2010). Interaction of non-coding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes & Development, 24(20), 2264–2269.

    Article  CAS  Google Scholar 

  • Shanker, S., Job, G., George, O. L., Creamer, K. M., Shaban, A., & Partridge, J. F. (2010). Continuous requirement for the Clr4 complex but not RNAi for centromeric heterochromatin assembly in fission yeast harboring a disrupted RITS complex. PLoS Genetics, 6(10), e1001174.

    Article  PubMed  CAS  Google Scholar 

  • Simon, M. D., Wang, C. I., Kharchenko, P. V., West, J. A., Chapman, B. A., Alekseyenko, A. A., et al. (2011). The genomic binding sites of a non-coding RNA. Proceedings of the National Academy of Sciences, 108(51), 20497–20502.

    Article  CAS  Google Scholar 

  • Sugiyama, T., & Sugioka-Sugiyama, R. (2011). Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO Journal, 30(6), 1027–1039.

    Article  PubMed  CAS  Google Scholar 

  • Taft, R. J., Simons, C., Nahkuri, S., Oey, H., Korbie, D. J., Mercer, T. R., et al. (2011). Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans. Nature Structural & Molecular Biology, 17(8), 1030–1034.

    Article  CAS  Google Scholar 

  • Tan-Wong, S. M., Zaugg, J. B., Camblong, J., Xu, Z., Zhang, D. W., Mischo, H. E., et al. (2012). Gene loops enhance transcriptional directionality. Science, 338, 671–675.

    Article  PubMed  CAS  Google Scholar 

  • Thebault, P., Boutin, G., Bhat, W., Rufiange, A., Martens, J., Nourani, A. (2011). Transcription regulation by the non-coding RNA SRG1 requires Spt2-dependent chromatin deposition in the wake of RNAP II. Molecular and Cellular Biology, doi:10.1128/MCB.01083-01010.

  • Thiebaut, M., Colin, J., Neil, H., Jacquier, A., Seraphin, B., Lacroute, F., et al. (2008). Futile cycle of transcription initiation and termination modulates the response to nucleotide shortage in S. cerevisiae. Molecular Cell, 31(5), 671–682.

    Article  PubMed  CAS  Google Scholar 

  • Uhler, J. P., Hertel, C., & Svejstrup, J. Q. (2007). A role for non-coding transcription in activation of the yeast PHO5 gene. Proceedings of the National Academy of Sciences of the United States of America, 104(19), 8011–8016.

    Article  PubMed  CAS  Google Scholar 

  • van Dijk, E. L., Chen, C. L., d/’Aubenton-Carafa, Y., Gourvennec, S., Kwapisz, M., Roche, V., et al. (2011). XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature, 475(7354), 114–117.

    Article  PubMed  CAS  Google Scholar 

  • van Werven Folkert, J., Neuert, G., Hendrick, N., Lardenois, A., Buratowski, S., van Oudenaarden, A., et al. (2012). Transcription of two long non-coding RNAs mediates mating-type control of gametogenesis in budding yeast. Cell, 150(6), 1170–1181.

    Article  PubMed  CAS  Google Scholar 

  • Vasiljeva, L., & Buratowski, S. (2006). Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Molecular Cell, 21(2), 239–248.

    Article  PubMed  CAS  Google Scholar 

  • Vasiljeva, L., Kim, M., Terzi, N., Soares, L. M., & Buratowski, S. (2008). Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Molecular Cell, 29(3), 313–323.

    Article  PubMed  CAS  Google Scholar 

  • Wahls, W. P., Siegel, E. R., & Davidson, M. K. (2008). Meiotic recombination hotspots of fission yeast are directed to loci that express non-coding RNA. PLoS ONE, 3(8), e2887.

    Article  PubMed  CAS  Google Scholar 

  • Wang, X., Arai, S., Song, X., Reichart, D., Du, K., Pascual, G., et al. (2008). Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature, 454(7200), 126–130.

    Article  PubMed  CAS  Google Scholar 

  • Wierzbicki, A. T., Haag, J. R., & Pikaard, C. S. (2008). Non-coding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell, 135(4), 635–648.

    Article  PubMed  CAS  Google Scholar 

  • Wierzbicki, A. T., Ream, T. S., Haag, J. R., & Pikaard, C. S. (2009). RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nature Genetics, 41(5), 630–634.

    Article  PubMed  CAS  Google Scholar 

  • Wierzbicki, A. T., Cocklin, R., Mayampurath, A., Lister, R., Rowley, M. J., Gregory, B. D., et al. (2012). Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes & Development, 26(16), 1825–1836.

    Article  CAS  Google Scholar 

  • Xu, Z., Wei, W., Gagneur, J., Perocchi, F., Clauder-Munster, S., Camblong, J., et al. (2009). Bidirectional promoters generate pervasive transcription in yeast. Nature, 457(7232), 1033–1037.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Z., Wei, W., Gagneur, J., Clauder-Munster, S., Smolik, M., Huber, W., et al. (2011). Antisense expression increases gene expression variability and locus interdependency. Molecular Systems Biology, 7, 1–10.

    Article  CAS  Google Scholar 

  • Yamanaka, S., Yamashita, A., Harigaya, Y., Iwata, R., & Yamamoto, M. (2010). Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO Journal, 29(13), 2173–2181.

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka, S., Mehta, S., Reyes-Turcu, F. E., Zhuang, F., Fuchs, R.T., Rong, Y., Robb, G. B., Grewal, S. I. (2012). RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature, 493, 557-560.

    Google Scholar 

  • Yang, L., Lin, C., Liu, W., Zhang, J., Ohgi Kenneth, A., Grinstein Jonathan, D., et al. (2011). ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell, 147(4), 773–788.

    Article  PubMed  CAS  Google Scholar 

  • Yassour, M., Pfiffner, J., Levin, J., Adiconis, X., Gnirke, A., Nusbaum, C., et al. (2010). Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biology, 11(8), R87.

    Article  PubMed  CAS  Google Scholar 

  • Young, R. S., Marques, A. C., Tibbit, C., Haerty, W., Bassett, A. R., Liu, J. L., et al. (2012). Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biology and Evolution, 4(4), 427–442.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, K., Fischer, T., Porter, R. L., Dhakshnamoorthy, J., Zofall, M., Zhou, M., et al. (2011). Clr4/Suv39 and RNA quality control factors cooperate to trigger RNAi and suppress antisense RNA. Science, 331(6024), 1624–1627.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, J., Ohsumi, T. K., Kung, J. T., Ogawa, Y., Grau, D. J., Sarma, K., et al. (2010). Genome-wide identification of polycomb-associated RNAs by RIP-seq. Molecular Cell, 40(6), 939–953.

    Article  PubMed  CAS  Google Scholar 

  • Zheng, Q., Rowley, M. J., Bohmdorfer, G., Sandhu, D., Gregory, B. D., Wierzbicki, A. T. (2012). RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant Journal, 10.1111/tpj.12034.

  • Zhong, X., Hale, C. J., Law, J. A., Johnson, L. M., Feng, S., Tu, A., et al. (2012). DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nature Structural & Molecular Biology, 19(9), 870–875.

    Article  CAS  Google Scholar 

  • Zhu, Y., Rowley, M. J., Böhmdorfer, G., Wierzbicki Andrzej, T. (2012). A SWI/SNF chromatin-remodeling complex acts in non-coding RNA-mediated transcriptional silencing. Molecular Cell, 49, 298-309.

    Google Scholar 

  • Zofall, M., Yamanaka, S., Reyes-Turcu, F. E., Zhang, K., Rubin, C., & Grewal, S. I. (2012). RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science, 335(6064), 96–100.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by Wellcome Trust [086587 and 077248]. Work in the Wellcome Trust Centre for Cell Biology is supported by Wellcome Trust core funding [092076].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Tollervey .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Tuck, A., Tollervey, D. (2013). Functions of Long Non-Coding RNAs in Non-mammalian Systems. In: Khalil, A., Coller, J. (eds) Molecular Biology of Long Non-coding RNAs. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8621-3_6

Download citation

Publish with us

Policies and ethics