1932

Abstract

Our understanding of the detailed molecular mechanisms underpinning adaptation is still poor. One example for which mechanistic understanding of regulation has converged with studies of life history variation is (). determines the need for plants to overwinter and their ability to respond to prolonged cold in a process termed vernalization. This review highlights how molecular analysis of vernalization pathways has revealed important insight into antisense-mediated chromatin silencing mechanisms that regulate . In turn, such insight has enabled molecular dissection of the diversity in vernalization across natural populations of . Changes in both cotranscriptional regulation and epigenetic silencing of are caused by noncoding polymorphisms at . The locus is therefore providing important concepts for how noncoding transcription and chromatin regulation influence gene expression and how these mechanisms can vary to underpin adaptation in natural populations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100616-060546
2017-10-06
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/33/1/annurev-cellbio-100616-060546.html?itemId=/content/journals/10.1146/annurev-cellbio-100616-060546&mimeType=html&fmt=ahah

Literature Cited

  1. Aebi M, Hornig H, Padgett RA, Reiser J, Weissmann C. 1986. Sequence requirements for splicing of higher eukaryotic nuclear pre-mRNA. Cell 47:555–65 [Google Scholar]
  2. Ågren J, Oakley CG, McKay JK, Lovell JT, Schemske DW. 2013. Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana. PNAS 110:21077–82 [Google Scholar]
  3. Aikawa S, Kobayashi MJ, Satake A, Shimizu KK, Kudoh H. 2010. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. PNAS 107:11632–37 [Google Scholar]
  4. Alexandre CM, Hennig L. 2008. FLC or not FLC: the other side of vernalization. J. Exp. Bot. 59:1127–35 [Google Scholar]
  5. Angel A, Song J, Dean C, Howard M. 2011. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476:105–8 [Google Scholar]
  6. Angel A, Song J, Yang H, Questa JI, Dean C, Howard M. 2015. Vernalizing cold is registered digitally at FLC. PNAS 112:201503100 [Google Scholar]
  7. Ausín I, Alonso-Blanco C, Jarillo JA, Ruiz-García L, Martínez-Zapater JM. 2004. Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36:162–66 [Google Scholar]
  8. Bentley DL. 2014. Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 15:163–75 [Google Scholar]
  9. Berr A, Xu L, Gao J, Cognat V, Steinmetz A. et al. 2009. SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151:1476–85 [Google Scholar]
  10. Berry S, Hartley M, Olsson TSG, Dean C, Howard M. 2015. Local chromatin environment of a Polycomb target gene instructs its own epigenetic inheritance. eLife 4:e07205 [Google Scholar]
  11. Bouché F, Detry N, Périlleux C. 2015. Heat can erase epigenetic marks of vernalization in Arabidopsis. Plant Signal. Behav. 10:e990799 [Google Scholar]
  12. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A. et al. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLOS Genet 6:e1000940 [Google Scholar]
  13. Burghardt LT, Runcie DE, Wilczek AM, Cooper MD, Roe JL. et al. 2016. Fluctuating, warm temperatures decrease the effect of a key floral repressor on flowering time in Arabidopsis thaliana. New Phytol. 210:564–76 [Google Scholar]
  14. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. 2004. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. PNAS 101:15670–75 [Google Scholar]
  15. Cao Y, Wen L, Wang Z, Ma L. 2015. SKIP interacts with the Paf1 complex to regulate flowering via activation of FLC transcription in Arabidopsis. Mol. Plant 8:1816–19 [Google Scholar]
  16. Castaings L, Bergonzi S, Albani MC, Kemi U, Savolainen O, Coupland G. 2014. Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives. Nat. Commun 5:4457 [Google Scholar]
  17. Choi K, Kim J, Hwang H-J, Kim S, Park C. et al. 2011. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23:289–303 [Google Scholar]
  18. Chouard P. 1960. Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11:191–238 [Google Scholar]
  19. Coustham V, Li P, Strange A, Lister C, Song J, Dean C. 2012. Quantitative modulation of Polycomb silencing underlies natural variation in vernalization. Science 337:584–87 [Google Scholar]
  20. Crevillén P, Dean C. 2011. Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr. Opin. Plant Biol. 14:38–44 [Google Scholar]
  21. Crevillén P, Sonmez C, Wu Z, Dean C. 2013. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J 32:140–48 [Google Scholar]
  22. Crevillén P, Yang H, Cui X, Greeff C, Trick M. et al. 2014. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515:587–90 [Google Scholar]
  23. Csorba T, Questa JI, Sun Q, Dean C. 2014. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. PNAS 111:16160–65 [Google Scholar]
  24. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M. et al. 2003. A slow RNA polymerase II affects alternative splicing in vivo. Mol. Cell 12:525–32 [Google Scholar]
  25. De Lucia F, Crevillen P, Jones AME, Greb T, Dean C. 2008. A PHD-Polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. PNAS 105:16831–36 [Google Scholar]
  26. Del Olmo I, López JA, Vázquez J, Raynaud C, Piñeiro M, Jarillo JA. 2016. Arabidopsis DNA polymerase ϵ recruits components of Polycomb repressor complex to mediate epigenetic gene silencing. Nucleic Acids Res 44:5597–614 [Google Scholar]
  27. Duncan S, Holm S, Questa J, Irwin J, Grant A, Dean C. 2015. Seasonal shift in timing of vernalization as an adaptation to extreme winter. eLife 4:e06620 [Google Scholar]
  28. Fang R, Moss WN, Rutenberg-Schoenberg M, Simon MD. 2015. Probing Xist RNA structure in cells using Targeted Structure-Seq. PLOS Genet 11:e1005668 [Google Scholar]
  29. Finnegan EJ, Dennis ES. 2007. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17:1978–83 [Google Scholar]
  30. Franks SJ, Sim S, Weis AE. 2007. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. PNAS 104:1278–82 [Google Scholar]
  31. Gan E-S, Xu Y, Wong J-Y, Goh JG, Sun B. et al. 2014. Jumonji demethylases moderate precocious flowering at elevated temperature via regulation of FLC in Arabidopsis. Nat. Commun. 5:5098 [Google Scholar]
  32. Geraldo N, Bäurle I, Kidou S-I, Hu X, Dean C. 2009. FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol 150:1611–18 [Google Scholar]
  33. Greb T, Mylne JS, Crevillen P, Geraldo N, An H. et al. 2007. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17:73–78 [Google Scholar]
  34. Grillo MA, Li C, Hammond M, Wang L, Schemske DW. 2013. Genetic architecture of flowering time differentiation between locally adapted populations of Arabidopsis thaliana. New Phytol. 197:1321–31 [Google Scholar]
  35. Grosveld F, van Assendelft GB, Greaves DR, Kollias G. 1987. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell 51:975–85 [Google Scholar]
  36. Gu X, Jiang D, Yang W, Jacob Y, Michaels SD, He Y. 2011. Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLOS Genet 7:e1002366 [Google Scholar]
  37. Halligan DL, Kousathanas A, Ness RW, Harr B, Eöry L. et al. 2013. Contributions of protein-coding and regulatory change to adaptive molecular evolution in murid rodents. PLOS Genet 9:e1003995 [Google Scholar]
  38. Hawkes EJ, Hennelly SP, Novikova IV, Irwin JA, Dean C. et al. 2016. COOLAIR antisense RNAs form evolutionarily conserved elaborate secondary structures. Cell Rep 16:3087–96 [Google Scholar]
  39. He Y, Doyle MR, Amasino RM. 2004. PAF1-complex-mediated histone methylation of FLOWERING LOCUSC chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18:2774–84 [Google Scholar]
  40. Helliwell CA, Robertson M, Finnegan EJ, Buzas DM, Dennis ES. 2011. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLOS ONE 6:e21513 [Google Scholar]
  41. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79 [Google Scholar]
  42. Hoffmann MH. 2005. Evolution of the realized climatic niche in the genus Arabidopsis (Brassicaceae). Evolution 59:1425–36 [Google Scholar]
  43. Hon GC, Hawkins RD, Ren B. 2009. Predictive chromatin signatures in the mammalian genome. Hum. Mol. Genet. 18:R195–201 [Google Scholar]
  44. Hornyik C, Terzi LC, Simpson GG. 2010. The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev. Cell 18:203–13 [Google Scholar]
  45. Hyun Y, Yun H, Park K, Ohr H, Lee O. et al. 2013. The catalytic subunit of Arabidopsis DNA polymerase α ensures stable maintenance of histone modification. Development 140:156–66 [Google Scholar]
  46. Johanson U. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–47 [Google Scholar]
  47. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E. et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61 [Google Scholar]
  48. Jung J-H, Park J-H, Lee S, To TK, Kim J-M. et al. 2013. The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–90 [Google Scholar]
  49. King M, Wilson A. 1975. Evolution at two levels in humans and chimpanzees. Science 188:107–16 [Google Scholar]
  50. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:345–70 [Google Scholar]
  51. Kornienko AE, Dotter CP, Guenzl PM, Gisslinger H, Gisslinger B. et al. 2016. Long non-coding RNAs display higher natural expression variation than protein-coding genes in healthy humans. Genome Biol 17:14 [Google Scholar]
  52. Kvitek DJ, Sherlock G. 2011. Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLOS Genet 7:e1002056 [Google Scholar]
  53. Lanzuolo C, Roure V, Dekker J, Bantignies F, Orlando V. 2007. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 9:1167–74 [Google Scholar]
  54. Lee H, Suh SS, Park E, Cho E, Ahn JH. et al. 2000. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14:2366–76 [Google Scholar]
  55. Lee I, Bleecker A, Amasino R. 1993. Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237:171–76 [Google Scholar]
  56. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D. 2005. Diversity of flowering responses in wild Arabidopsis thaliana strains. PLOS Genet 1:109–18 [Google Scholar]
  57. Li B, Carey M, Workman JL. 2007. The role of chromatin during transcription. Cell 128:707–19 [Google Scholar]
  58. Li P, Filiault D, Box MS, Kerdaffrec E, van Oosterhout C. et al. 2014. Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes Dev 28:1635–40 [Google Scholar]
  59. Li P, Tao Z, Dean C. 2015. Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR. Genes Dev. 29:696–701 [Google Scholar]
  60. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. 2010. Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97 [Google Scholar]
  61. Losos B. 2011. Convergence, adaptation, and constraint. Evolution 65:1827–40 [Google Scholar]
  62. Maison C, Bailly D, Peters AHFM, Quivy J-P, Roche D. et al. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329–34 [Google Scholar]
  63. Margueron R, Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature 469:343–49 [Google Scholar]
  64. Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C. 2014. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol. Cell 54:156–65 [Google Scholar]
  65. Mercer TR, Dinger ME, Mattick JS. 2009. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10:155–59 [Google Scholar]
  66. Michaels SD. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–56 [Google Scholar]
  67. Michaels SD, He Y, Scortecci KC, Amasino RM. 2003. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. PNAS 100:10102–7 [Google Scholar]
  68. Myers RM, Tilly K, Maniatis T. 1986. Fine structure genetic analysis of a beta-globin promoter. Science 232:613–18 [Google Scholar]
  69. Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L. et al. 2006. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. PNAS 103:5012–17 [Google Scholar]
  70. Napp-Zinn K. 1957. Untersuchungen zur Genetik des Kältebedürfnisses bei Arabidopsis thaliana. Z. Indukt. Abstamm. Vererb. 88:253–85 [Google Scholar]
  71. Nordborg M, Bergelson J. 1999. The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. Am. J. Bot. 86:470–75 [Google Scholar]
  72. Parcy F. 2005. Flowering: a time for integration. Int. J. Dev. Biol. 49:585–93 [Google Scholar]
  73. Pien S, Fleury D, Mylne JS, Crevillen P, Inzé D. et al. 2008. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20:580–88 [Google Scholar]
  74. Qüesta JI, Song J, Geraldo N, An H, Dean C. 2016. Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science 353:485–88 [Google Scholar]
  75. Quinn JJ, Zhang QC, Georgiev P, Ilik IA, Akhtar A, Chang HY. 2016. Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Genes Dev 30:191–207 [Google Scholar]
  76. Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards CM. 2007. Evolutionary conservation of the FLOWERING LOCUS C–mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307 [Google Scholar]
  77. Rosa S, De Lucia F, Mylne JS, Zhu D, Ohmido N. et al. 2013. Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev 27:1845–50 [Google Scholar]
  78. Rosa S, Duncan S, Dean C. 2016. Mutually exclusive sense-antisense transcription at FLC facilitates environmentally induced gene repression. Nat. Commun. 7:13031 [Google Scholar]
  79. Scarcelli N, Cheverud JM, Schaal BA, Kover PX. 2007. Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. PNAS 104:16986–91 [Google Scholar]
  80. Searle I, He Y, Turck F, Vincent C, Fornara F. et al. 2006. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20:898–912 [Google Scholar]
  81. Sheldon CC. 1999. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–58 [Google Scholar]
  82. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES. 2000. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). PNAS 97:3753–58 [Google Scholar]
  83. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C. et al. 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138:1163–73 [Google Scholar]
  84. Shindo C, Lister C, Crevillen P, Nordborg M, Dean C. 2006. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev 20:3079–83 [Google Scholar]
  85. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LE. et al. 2013. Extensive natural epigenetic variation at a de novo originated gene. PLOS Genet 9:e1003437 [Google Scholar]
  86. Simpson GG, Dean C. 2002. Arabidopsis, the Rosetta stone of flowering time. Science 296:285–89 [Google Scholar]
  87. Somarowthu S, Legiewicz M, Chillón I, Marcia M, Liu F, Pyle AM. 2015. HOTAIR forms an intricate and modular secondary structure. Mol. Cell 58:353–61 [Google Scholar]
  88. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C. et al. 2004. A latitudinal cline in flowering time in Arabidopsisthaliana modulated by the flowering time gene FRIGIDA. PNAS 101:4712–17 [Google Scholar]
  89. Strange A, Li P, Lister C, Anderson J, Warthmann N. et al. 2011. Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLOS ONE 6:e19949 [Google Scholar]
  90. Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C. 2013. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340:619–21 [Google Scholar]
  91. Sung S, Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–64 [Google Scholar]
  92. Sung S, He Y, Eshoo TW, Tamada Y, Johnson L. et al. 2006. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38:706–10 [Google Scholar]
  93. Swiezewski S, Crevillen P, Liu F, Ecker JR, Jerzmanowski A, Dean C. 2007. Small RNA–mediated chromatin silencing directed to the 3′ region of the Arabidopsis gene encoding the developmental regulator, FLC. PNAS 104:3633–38 [Google Scholar]
  94. Swiezewski S, Liu F, Magusin A, Dean C. 2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802 [Google Scholar]
  95. Stern DL. 2013. The genetic causes of convergent evolution. Nat. Rev. Genet. 14:751–64 [Google Scholar]
  96. Stern DL, Orgogozo V. 2008. The loci of evolution: How predictable is genetic evolution?. Evolution 62:2155–77 [Google Scholar]
  97. Turck F, Roudier F, Farrona S, Martin-Magniette M-L, Guillaume E. et al. 2007. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLOS Genet 3:e86 [Google Scholar]
  98. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. 2011. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147:1537–50 [Google Scholar]
  99. van Bakel H, Nislow C, Blencowe BJ, Hughes TR. 2010. Most “dark matter” transcripts are associated with known genes. PLOS Biol 8:e1000371 [Google Scholar]
  100. Wang R, Farrona S, Vincent C, Joecker A, Schoof H. et al. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–27 [Google Scholar]
  101. Wang Y, Gu X, Yuan W, Schmitz RJ, He Y. 2014. Photoperiodic control of the floral transition through a distinct polycomb repressive complex. Dev. Cell 28:727–36 [Google Scholar]
  102. Wellmer F, Riechmann JL. 2010. Gene networks controlling the initiation of flower development. Trends Genet 26:519–27 [Google Scholar]
  103. Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D. 2005. FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170:1197–207 [Google Scholar]
  104. Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA. 2006. The Arabidopsisthaliana vernalization response requires a Polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. PNAS 103:14631–36 [Google Scholar]
  105. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206–16 [Google Scholar]
  106. Wu Z, Ietswaart R, Liu F, Yang H, Howard M, Dean C. 2016. Quantitative regulation of FLC via coordinated transcriptional initiation and elongation. PNAS 113:218–23 [Google Scholar]
  107. Yang H, Howard M, Dean C. 2014. Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr. Biol. 24:1793–97 [Google Scholar]
  108. Yang H, Howard M, Dean C. 2016. Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC. PNAS 113:9369–74 [Google Scholar]
  109. Yanofsky C. 1971. Tryptophan biosynthesis in Escherichia coli. Genetic determination of the proteins involved. JAMA 218:1026–35 [Google Scholar]
  110. Yanofsky C. 1981. Attenuation in the control of expression of bacterial operons. Nature 289:751–58 [Google Scholar]
  111. Young MD, Willson TA, Wakefield MJ, Trounson E, Hilton DJ. et al. 2011. ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res 39:7415–27 [Google Scholar]
  112. Yun H, Hyun Y, Kang MJ, Noh YS, Noh B, Choi Y. 2011. Identification of regulators required for the reactivation of FLOWERING LOCUS C during Arabidopsis reproduction. Planta 234:1237–50 [Google Scholar]
  113. Zaratiegui M, Castel SE, Irvine DV, Kloc A, Ren J. et al. 2011. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479:135–38 [Google Scholar]
  114. Zhang X, Rice K, Wang Y, Chen W, Zhong Y. et al. 2010. Maternally expressed gene 3 (MEG3) noncoding ribonucleic acid: isoform structure, expression, and functions. Endocrinology 151:939–47 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100616-060546
Loading
/content/journals/10.1146/annurev-cellbio-100616-060546
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error