Message ends: RNA 3′ processing and flowering time control

Journal of Experimental Botany

Volumn 65, Issue 2, 2014, Pages 353-363

  Rataj, Katarzyna ^a   Simpson, Gordon G ^a,b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MESSENGER RNA; VEGETABLE PROTEIN;

ARTICLE; FLOWER; GENETICS; METABOLISM; PHYSIOLOGY; RNA PROCESSING; TIME;

FLOWERS; PLANT PROTEINS; RNA 3' END PROCESSING; RNA, ANTISENSE; RNA, MESSENGER; TIME FACTORS;

EID: 84893334606     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert439     Document Type: Article

References (78)

1. Adams S, Allen T, Whitelam GC. 2009. Interaction between the light quality and flowering time pathways in Arabidopsis. The Plant Journal 60, 257-267.
2. Ali GS, Palusa SG, Golovkin M, Prasad J, Manley JL, Reddy ASN. 2007. Regulation of plant developmental processes by a novel splicing factor. PLoS ONE 2, e471.
3. Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13, 627-639.
4. Ansari A, Hampsey M. 2005. A role for the CPF 3′-end processing machinery in RNAP II-dependent gene looping. Genes & Development 19, 2969-2978.
5. Ariyoshi M, Schwabe JWR. 2003. A conserved structural motif reveals the essential transcriptional repression function of Spen proteins and their role in developmental signaling. Genes & Development 17, 1909-1920.
6. Aukerman MJ, Sakai H. 2003. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15, 2730-2741.
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. Nature Genetics 36, 162-166.
8. Bäurle I, Dean C. 2008. Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3, e2733.
9. Bäurle I, Smith L, Baulcombe DC, Dean C. 2007. Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318, 109-112.
10. Bergonzi S, Albani MC, Loren van Themaat EV, Nordstrom KJV, Wang R, Schneeberger K, Moerland PD, Coupland G. 2013. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340, 1094-1097.
11. Bezerra IC, Michaels SD, Schomburg FM, Amasino RM. 2004. Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. The Plant Journal 40, 112-119.
12. Bin Tian, Manley JL. 2013. Alternative cleavage and polyadenylation: the long and short of it. Trends in Biochemical Sciences 38, 312-320.
13. Castelnuovo M, Rahman S, Guffanti E, Infantino V, Stutz F, Zenklusen D. 2013. Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nature Structural & Molecular Biology 20, 851-858.
14. Chekanova JA, Gregory BD, Reverdatto SV, et al. 2007. Genomewide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131, 1340-1353.
15. 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, 584-587.
16. Crisucci EM, Arndt KM. 2012. Paf1 restricts Gcn4 occupancy and antisense transcription at the ARG1 promoter. Molecular and Cellular Biology 32, 1150-1163.
17. Duc C, Sherstnev A, Cole C, Barton GJ, Simpson GG. 2013. Transcription termination and chimeric rna formation controlled by Arabidopsis thaliana FPA. PLoS Genetics 9, e1003867.
18. 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 Physiology 150, 1611-1618.
19. Ginno PA, Lim YW, Lott PL, Korf IF, Chedin F. 2013. GC skew at the 5′ and 3′ ends of human genes links R-loop formation to epigenetic regulation and transcription termination. Genome Research 23, 1590-1600.
20. 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.
21. Henderson IR, Liu F, Drea S, Simpson GG, Dean C. 2005. An allelic series reveals essential roles for FY in plant development in addition to flowering-time control. Development 132, 3597-3607.
22. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79.
23. Hornyik C, Duc C, Rataj K, Terzi LC, Simpson GG. 2010a. Alternative polyadenylation of antisense RNAs and flowering time control. Biochemical Society Transactions 38, 1077-1081.
24. Hornyik C, Terzi LC, Simpson GG. 2010b. The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Developmental Cell 18, 203-213.
25. Huijser P, Schmid M. 2011. The control of developmental phase transitions in plants. Development 138, 4117-4129.
26. Jacquier A. 2009. The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nature Reviews Genetics 10, 833-844.
27. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344-347.
28. Koornneef M, Hanhart CJ, van der Veen JH. 1991. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular & General Genetics 229, 57-66.
29. Kornblihtt AR, Schor IE, Allo M, Blencowe BJ. 2009. When chromatin meets splicing. Nature Structural & Molecular Biology 16, 902-903.
30. Kuhn JM, Breton G, Schroeder JI. 2007. mRNA metabolism of flowering-time regulators in wild-type Arabidopsis revealed by a nuclear cap binding protein mutant, abh1. The Plant Journal 50, 1049-1062.
31. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, Rätsch G, Weigel D. 2008. Dual roles of the nuclear capbinding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 105, 8795-8800.
32. Lee JH, Ryu H-S, Chung KS, Posé D, Kim S, Schmid M, Ahn JH. 2013. Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342, 628-632.
33. Lim M-H, Kim J, Kim Y-S, Chung K-S, Seo Y-H, Lee I, Kim J, Hong CB, Kim H-J, Park C-M. 2004. A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16, 731-740.
34. 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.
35. Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C. 2007. The Arabidopsis RNA-binding protein FCA requires a lysinespecific demethylase 1 homolog to downregulate FLC. Molecular Cell 28, 398-407.
36. Lyons R, Iwase A, Gänsewig T, et al. 2013. The RNA-binding protein FPA regulates flg22-triggered defense responses and transcription factor activity by alternative polyadenylation. Scientific Reports 3, 2866.
37. Macknight R, Bancroft I, Page T, et al. 1997. FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737-745.
38. Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C. 2002. Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14, 877-888.
39. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956.
40. Michaels SD, Amasino RM. 2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935-941.
41. Mockler TC, Yu X, Shalitin D, et al. 2004. Regulation of flowering time in Arabidopsis by K homology domain proteins. Proceedings of the National Academy of Sciences, USA 101, 12759-12764.
42. Nagaike T, Logan C, Hotta I, Rozenblatt-Rosen O, Meyerson M, Manley JL. 2011. Transcriptional activators enhance polyadenylation of mRNA precursors. Molecular Cell 41, 409-418.
43. Niwa M, Rose SD, Berget SM. 1990. In vitro polyadenylation is stimulated by the presence of an upstream intron. Genes & Development 4, 1552-1559.
44. Ohnacker M, Barabino SM, Preker PJ, Keller W. 2000. The WD-repeat protein pfs2p bridges two essential factors within the yeast pre-mRNA 3′-end-processing complex. EMBO Journal 19, 37-47.
45. O'Sullivan JM, Tan-Wong SM, Morillon A, Lee B, Coles J, Mellor J, Proudfoot NJ. 2004. Gene loops juxtapose promoters and terminators in yeast. Nature Genetics 36, 1014-1018.
46. Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RGH, Schmid M. 2013. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503, 414-417.
47. Quesada V, Macknight R, Dean C, Simpson GG. 2003. Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO Journal 22, 3142-3152.
48. Ripoll JJ, Ferrándiz C, Martínez-Laborda A, Vera A. 2006. PEPPER, a novel K-homology domain gene, regulates vegetative and gynoecium development in Arabidopsis. Developmental Biology 289, 346-359.
49. Ripoll JJ, Rodríguez-Cazorla E, González-Reig S, Andújar A, Alonso-Cantabrana H, Perez-Amador MA, Carbonell J, Martínez-Laborda A, Vera A. 2009. Antagonistic interactions between Arabidopsis K-homology domain genes uncover PEPPER as a positive regulator of the central floral repressor FLOWERING LOCUS C. Developmental Biology 333, 251-262.
50. Rozenblatt-Rosen O, Nagaike T, Francis JM, Kaneko S, Glatt KA, Hughes CM, LaFramboise T, Manley JL, Meyerson M. 2009. The tumor suppressor Cdc73 functionally associates with CPSF and CstF 3′ mRNA processing factors. Proceedings of the National Academy of Sciences, USA 106, 755-760.
51. Ruelens P, de Maagd RA, Proost S, en GUNTS, Geuten K, Kaufmann K. 2013. FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nature Communications 4, 2280.
52. Saze H, Kitayama J, Takashima K, Miura S, Harukawa Y, Ito T, Kakutani T. 2013. Mechanism for full-length RNA processingof Arabidopsis genes containing intragenic heterochromatin. Nature Communications 4, 2301.
53. Schomburg FM, Patton DA, Meinke DW, Amasino RM. 2001. FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13, 1427-1436.
54. Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G. 2006. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes & Development 20, 898-912.
55. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES. 1999. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445-458.
56. Sheldon KE, Mauger DM, Arndt KM. 2005. A requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 3′ end formation. Molecular Cell 20, 225-236.
57. Sherstnev A, Duc C, Cole C, Zacharaki V, Hornyik C, Ozsolak F, Milos PM, Barton GJ, Simpson GG. 2012. Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nature Structural & Molecular Biology 19, 845-852.
58. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, Yates JR, Frank J, Manley JL. 2009. Molecular architecture of the human pre-mRNA 3′ processing complex. Molecular Cell 33, 365-376.
59. Simpson GG. 2004. The autonomous pathway: epigenetic and posttranscriptional gene regulation in the control of Arabidopsis flowering time. Current Opinion in Plant Biology 7, 570-574.
60. Simpson GG, Dean C. 2002. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285-289.
61. Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C. 2003. FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113, 777-787.
62. Simpson GG, Laurie RE, Dijkwel PP, Quesada V, Stockwell PA, Dean C, Macknight RC. 2010. Noncanonical translation initiation of the Arabidopsis flowering time and alternative polyadenylation regulator FCA. Plant Cell 22, 3764-3777.
63. Skourti-Stathaki K, Proudfoot NJ, Gromak N. 2011. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Molecular Cell 42, 794-805.
64. Sonmez C, Bäurle I, Magusin A, Dreos R, Laubinger S, Weigel D, Dean C. 2011. RNA 3′ processing functions of Arabidopsis FCA and FPA limit intergenic transcription. Proceedings of the National Academy of Sciences, USA 108, 8508-8513.
65. Streitner C, Danisman S, Wehrle F, Schöning JC, Alfano JR, Staiger D. 2008. The small glycine-rich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. The Plant Journal 56, 239-250.
66. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE. 2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352-364.
67. 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, 619-621.
68. Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM. 2006. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nature Genetics 38, 706-710.
69. Swiezewski S, Crevillén 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. Proceedings of the National Academy of Sciences, USA 104, 3633-3638.
70. 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.
71. Tan-Wong SM, Wijayatilake HD, Proudfoot NJ. 2009. Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes & Development 23, 2610-2624.
72. 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.
73. Taoka K-I, Ohki I, Tsuji H, Kojima C, Shimamoto K. 2013. Structure and function of florigen and the receptor complex. Trends in Plant Science 18, 287-294.
74. Uhler JP, Hertel C, Svejstrup JQ. 2007. A role for noncoding transcription in activation of the yeast PHO5 gene. Proceedings of the National Academy of Sciences, USA 104, 8011-8016.
75. Wang C, Tian Q, Hou Z, Mucha M, Aukerman M, Olsen O-A. 2007. The Arabidopsis thaliana AT PRP39-1 gene, encoding a tetratricopeptide repeat protein with similarity to the yeast pre-mRNA processing protein PRP39, affects flowering time. Plant Cell Reports 26, 1357-1366.
76. Xing D, Zhao H, Xu R, Li QQ. 2008. Arabidopsis PCFS4, a homologue of yeast polyadenylation factor Pcf11p, regulates FCA alternative processing and promotes flowering time. The Plant Journal 54, 899-910.
77. Yu X, Michaels SD. 2010. The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLOWERING LOCUS C chromatin. Plant Physiology 153, 1074-1084.
78. Zhang Z, Fu J, Gilmour DS. 2005. CTD-dependent dismantling of the RNA polymerase II elongation complex by the pre-mRNA 3′-end processing factor, Pcf11. Genes & Development 19, 1572-1580.