Advertisement

Regulation of Flowering Time by RNA Processing

Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 326)

Plants control the time at which they flower by integrating environmental cues such as day length and temperature with an endogenous program of development. Flowering time is a quantitative trait and a model for how precision in gene regulation is delivered. In this review, we reveal that flowering time control is particularly rich in RNA processing-based gene regulatory phenomena. We review those factors which function in conserved RNA processing events like alternative 3′ end formation, splicing, RNA export and miRNA biogenesis and how they affect flowering time. Likewise, we review the novel plant-specific RNA-binding proteins identified as regulators of flowering time control. In addition, we add to the network of flowering time control pathways, information on alternative processing of flowering time gene pre-mRNAs. Finally, we describe new approaches to dissect the mechanisms which underpin this control.

Keywords

Flowering Time Curr Opin Cell Biol Short Vegetative Phase SQUAMOSA Promoter Binding Protein Like Thermal Induction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Achard P, Herr, A Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365PubMedCrossRefGoogle Scholar
  2. Arciga-Reyes L, Wootton L, Kieffer A, Davies B (2006) UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J 47:480–489PubMedCrossRefGoogle Scholar
  3. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741PubMedCrossRefGoogle Scholar
  4. Ausin I, Alonso-Blanco C, Martinez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705PubMedCrossRefGoogle Scholar
  5. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genetics 2:e106PubMedCrossRefGoogle Scholar
  6. Bezerra I C, Michaels SD, Schomburg FM, Amasino RM (2004) Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. Plant J 40:112–119PubMedCrossRefGoogle Scholar
  7. Blazquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171PubMedCrossRefGoogle Scholar
  8. Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281:1001–1005PubMedCrossRefGoogle Scholar
  9. Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P. (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377PubMedCrossRefGoogle Scholar
  10. Chen X (2004) A MicroRNA as a translational repressor of APETALA2 in arabidopsis flower development. Science 303:2022–2025PubMedCrossRefGoogle Scholar
  11. Chen X (2005) microRNA biogenesis and function in plants. FEBS Lett 579:5923–5931PubMedCrossRefGoogle Scholar
  12. Chen YI, Maika SD, Stevens SW (2006) Epitope tagging of proteins at the native chromosomal loci of genes in mice and in cultured vertebrate cells. J Mol Biol 361:412–419PubMedCrossRefGoogle Scholar
  13. Cheng Y, Kato N, Wang W, Li J, Chen X (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4:53–66PubMedCrossRefGoogle Scholar
  14. Cole CN, Scarcelli JJ (2006) Transport of messenger RNA from the nucleus to the cytoplasm. Curr Opin Cell Biol 18:299–306PubMedCrossRefGoogle Scholar
  15. Doerks T, Copley RR, Schultz J, Ponting CP, Bork P (2002) Systematic identification of novel protein domain families associated with nuclear functions. Genome Res 12:47–56PubMedCrossRefGoogle Scholar
  16. Dong C H, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26:9533–9543PubMedCrossRefGoogle Scholar
  17. Doyle MR, Bizzell CM, Keller MR, Michaels SD, Song J, Noh YS, Amasino RM (2005). HUA2 is required for the expression of floral repressors in Arabidopsis thaliana. Plant J 41:376–385PubMedCrossRefGoogle Scholar
  18. Elliott BJ, Dattaroy T, Meeks-Midkiff LR, Forbes KP, Hunt AG (2003). An interaction between an Arabidopsis poly(A) polymerase and a homologue of the 100 kDa subunit of CPSF. Plant Mol Biol 51:373–384PubMedCrossRefGoogle Scholar
  19. Golden TA, Schauer SE, Lang JD, Pien S, Mushegian AR, Grossniklaus U, Meinke DW, Ray A (2002) SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol 130:808–822PubMedCrossRefGoogle Scholar
  20. Golovkin M, Reddy AS (1999) An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1–70K protein. J Biol Chem 274:36428–36438PubMedCrossRefGoogle Scholar
  21. Golovkin G Reddy ASN (1998) The plant U1 small nuclear ribonucleoprotein particle 70 K protein interacts with two novel serine/arginine-rich proteins. Plant Cell 10:1637–1648PubMedCrossRefGoogle Scholar
  22. Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong, D, Stevenson, B, Zhu JK (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267PubMedCrossRefGoogle Scholar
  23. Gong Z Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu J-K (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci USA 99:11507–11512PubMedCrossRefGoogle Scholar
  24. Grigg SP, Canales C, Hay A, Tsiantis G (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437:1022–1026PubMedCrossRefGoogle Scholar
  25. 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 132:3597–3607PubMedCrossRefGoogle Scholar
  26. Herr AJ, Molnar A, Jones A, Baulcombe DC (2006) Defective RNA processing enhances RNA silencing and influences flowering of Arabidopsis. Proc Natl Acad Sci USA 103:14994–15001PubMedCrossRefGoogle Scholar
  27. Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487PubMedCrossRefGoogle Scholar
  28. Jones-Rhoades MW, Bartel DP, Bartel, B. (2006). MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefGoogle Scholar
  29. Kalyna K, Lopato S, Barta A (2003). Ectopic expression of atRSZ33 reveals its function in splicing and causes pleiotropic changes in development. Mol Biol Cell 14:3565–3577PubMedCrossRefGoogle Scholar
  30. Kim SH, Lin RJ (1996). Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol Cell Biol 16:6810–6819PubMedGoogle Scholar
  31. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385PubMedCrossRefGoogle Scholar
  32. Komuro A, Saeki K, Kato S (1999) Association of two nuclear proteins, Npw38 and NpwBP, via the interaction between the WW domain and a novel proline-rich motif containing glycine and arginine. J Biol Chem 274:36513–36519PubMedCrossRefGoogle Scholar
  33. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758PubMedCrossRefGoogle Scholar
  34. Lee JH, Cho YS, Yoon HS, Suh MC, Moon J, Lee I, Weigel D, Yun CH, Kim JK (2005) Conservation and divergence of FCA function between Arabidopsis and rice. Plant Mol Biol 58:823–838PubMedCrossRefGoogle Scholar
  35. Lee JH, Yoo SJ, Park SH, Hwang, I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21:397–402PubMedCrossRefGoogle Scholar
  36. Lim RY, Fahrenkrog B (2006) The nuclear pore complex up close. Curr Opin Cell Biol 18:342–347PubMedCrossRefGoogle Scholar
  37. Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058PubMedCrossRefGoogle Scholar
  38. Lockhart SR, Rymond BC (1994) Commitment of yeast pre-mRNA to the splicing pathway requires a novel U1 small nuclear ribonucleoprotein polypeptide, Prp39p. Mol Cell Biol 14:3623–3633PubMedGoogle Scholar
  39. Loiodice I, Alves A, Rabut G, Van Overbeek L, Ellenberg J, Sibarita JB, Doye V (2004) The entire Nup107–160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol Biol Cell 15:3333–3344PubMedCrossRefGoogle Scholar
  40. Lopato S, Forstner C, Kalyna L, Hilscher J, Langhammer U, Indrapichate K, Lorkovic´ Z J, Barta A (2002) Network of interactions of a novel plant-specific Arg/Ser-rich protein, atRSZ33, with atSC35-like splicing factors. J Biol Chem 277:39989–39998PubMedCrossRefGoogle Scholar
  41. Lopato S, Kalyna L, Dorner S, Kobayashi R, Krainer AR, Barta A (1999) atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev 13:987–1001PubMedCrossRefGoogle Scholar
  42. Lorkovic´ ZJ, Wieczorek Kirk DA, Lambermon MH, Filipowicz W (2000) Pre-mRNA splicing in higher plants. Trends Plant Sci 5:160–167PubMedCrossRefGoogle Scholar
  43. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737–745PubMedCrossRefGoogle Scholar
  44. Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, Tong L (2006) Polyadenylation factor CPSF-73 is the pre-mRNA 3o-end-processing endonuclease. Nature 444:953–956PubMedCrossRefGoogle Scholar
  45. Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12:1612–1619PubMedCrossRefGoogle Scholar
  46. Mockler TC, Yu X, Shalitin D, Parikh D, Michael TP, Liou J, Huang J, Smith Z, Alonso JM, Ecker JR et al. (2004). Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci USA 101:12759–12764PubMedCrossRefGoogle Scholar
  47. Noh Y.-S, Bizzell CM, Noh B, Schomburg FM, Amasino RM (2004) EARLY FLOWERING 5 acts as a floral repressor in Arabidopsis. Plant J 38:664–672PubMedCrossRefGoogle Scholar
  48. Ohnacker O, 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 J 19:37–47PubMedCrossRefGoogle Scholar
  49. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  50. Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495PubMedCrossRefGoogle Scholar
  51. Parry G, Ward S, Cernac A, Dharmasiri S, Estelle P (2006) The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signaling and development. Plant Cell 18:1590–1603PubMedCrossRefGoogle Scholar
  52. Penheiter KL, Washburn TM, Porter SE, Hoffman MG, Jaehning JA (2005) A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol Cell 20:213–223PubMedCrossRefGoogle Scholar
  53. Proudfoot N (2004) New perspectives on connecting messenger RNA 3d end formation to transcription. Curr Opin Cell Biol 16:272–278PubMedCrossRefGoogle Scholar
  54. Quesada V, Dean C, Simpson GG (2005) Regulated RNA processing in the control of Arabidopsis flowering. Int J Dev Biol 49:773–780PubMedCrossRefGoogle Scholar
  55. Quesada V, Macknight R, Dean C, Simpson GG (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J 22:3142–3152PubMedCrossRefGoogle Scholar
  56. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425PubMedCrossRefGoogle Scholar
  57. Reddy ASN (2004) Plant serine/arginine-rich proteins and their role in pre-mRNA splicing. Trends Plant Sci 9:541–547PubMedCrossRefGoogle Scholar
  58. Samach A, Wigge PA (2005) Ambient temperature perception in plants. Curr Opin Plant Biol 8:483–486PubMedCrossRefGoogle Scholar
  59. Schmid S, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130:6001–6012PubMedCrossRefGoogle Scholar
  60. Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132:5471–5478PubMedCrossRefGoogle Scholar
  61. 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 13:1427–1436PubMedCrossRefGoogle Scholar
  62. Schwab R, Palatnik JF, Riester S, Schommer C, Schmid M, Weigel D (2005). Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527PubMedCrossRefGoogle Scholar
  63. Scortecci K, Michaels SD, Amasino RM (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol Biol 52:915–922PubMedCrossRefGoogle Scholar
  64. Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS S that represses flowering. Plant J 26:229–236PubMedCrossRefGoogle Scholar
  65. Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537PubMedCrossRefGoogle Scholar
  66. Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C (2003) FY Is an RNA 3j end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113:777–787PubMedCrossRefGoogle Scholar
  67. Sommer P, Nehrbass U (2005) Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore. Curr Opin Cell Biol 17:294–301PubMedCrossRefGoogle Scholar
  68. Sunkar R, Girke T, Jain PK, Zhu J-K (2005) Cloning and characterization of MICRORNAS from rice. Plant Cell 17:1397–1411PubMedCrossRefGoogle Scholar
  69. Teigelkamp S, McGarvey T, Plumpton M, Beggs JD (1994) The splicing factor PRP2, a putative RNA helicase, interacts directly with pre-mRNA. EMBO J 13:888–897PubMedGoogle Scholar
  70. Thomas B (2006) Light signals and flowering. J Exp Bot 57:3387–3393PubMedCrossRefGoogle Scholar
  71. Vazquez F, Gasciolli V, Crete P, Vaucheret H. (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351PubMedGoogle Scholar
  72. Vijayraghavan U, Company V, Abelson J (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev 3:1206–1216PubMedCrossRefGoogle Scholar
  73. Wang BB, and Brendel V (2006) Molecular characterization and phylogeny of U2AF35 homologs in plants. Plant Physiol 140:624–636PubMedCrossRefGoogle Scholar
  74. Wang C, Tian Q, Hou Z, Mucha M, Aukerman M, Olsen OA (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 Rep 26:1357–1366PubMedCrossRefGoogle Scholar
  75. Waragai W, Junn E, Kajikawa M, Takeuchi S, Kanazawa I, Shibata M, Mouradian MM, Okazawa H (2000) PQBP-1/Npw38, a nuclear protein binding to the polyglutamine tract, interacts with U5–15kD/dim1p via the carboxyl-terminal domain. Biochem Biophys Res Commun 273:592–595PubMedCrossRefGoogle Scholar
  76. 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 170:1197–1207PubMedCrossRefGoogle Scholar
  77. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547PubMedCrossRefGoogle Scholar
  78. Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154PubMedCrossRefGoogle Scholar
  79. Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850PubMedCrossRefGoogle Scholar
  80. Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  1. 1.Scottish Crop Research InstituteUK
  2. 2.Division of Plant Sciences, College of Life SciencesDundee University at SCRIScotland, UK
  3. 3.Genetics ProgrammeSCRIScotland, UK

Personalised recommendations

Cite chapter

Buy options