Circadian rhythms and post-transcriptional regulation in higher plants

Frontiers in Plant Science

Volumn 6, Issue June, 2015, Pages

  Romanowski, Andrés ^a   Yanovsky, Marcelo J ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

Alternative splicing; Arabidopsis thaliana; Circadian rhythms; MRNA nuclear export; Polyadenilation; Post transcriptional regulation; Regulation of translation; RNA turnover

Indexed keywords

ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 84935876729     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00437     Document Type: Article

References (111)

1. Addepalli, B., Meeks, L. R., Forbes, K. P., and Hunt, A. G. (2004). Novel alternative splicing of mRNAs encoding poly(A) polymerases in Arabidopsis. Biochim. Biophys. Acta 1679, 117-128.Doi: 10.1016/j.bbaexp.2004.06.001.
2. Beckwith, E. J., and Yanovsky, M. J. (2014). Circadian regulation of gene expression: at the crossroads of transcriptional and post-transcriptional regulatory networks. Curr. Opin. Genet. Dev. 27, 35-42.Doi: 10.1016/j.gde. 2014.03.007.
3. Belostotsky, D. A., and Sieburth, L. E. (2009). Kill the messenger: mRNA decay and plant development. Curr. Opin. Plant Biol. 12, 96-102.Doi: 10.1016/j.pbi.2008.09.003.
4. Brown, S. A., Kowalska, E., and Dallmann, R. (2012). Reinventing the circadian feedback loop. Dev. Cell 22, 477-487.Doi: 10.1016/j.devcel.2012.02.007.
5. Calixto, C. P., Waugh, R., and Brown, J. W. (2015). Evolutionary relationships among barley and Arabidopsis core circadian clock and clock-associated genes. J. Mol. Evol. 80, 108-119.Doi: 10.1007/s00239-015-9665-0.
6. Chow, B. Y., Helfer, A., Nusinow, D. A., and Kay, S. A. (2012). ELF3 recruitment to the PRR9 promoter requires other evening complex members in the Arabidopsis circadian clock. Plant Signal. Behav. 7, 170-173.Doi: 10.4161/psb.18766.
7. Chow, B. Y., and Kay, S. A. (2013). Global approaches for telling time: omics and the Arabidopsis circadian clock. Semin. Cell Dev. Biol. 24, 383-392.Doi: 10.1016/j.semcdb.2013.02.005.
8. Cohen-Steiner, D., Edelsbrunner, H., Harer, J., and Mileyko, Y. (2010). Lipschitz functions have L p-stable persistence. Found. Comput. Math. 10, 127-139.Doi: 10.1007/s10208-010-9060-6.
9. Coon, S. L., Munson, P. J., Cherukuri, P. F., Sugden, D., Rath, M. F., Moller, M., et al. (2012). Circadian changes in long noncoding RNAs in the pineal gland. Proc. Natl. Acad. Sci. U.S.A. 109, 13319-13324.Doi: 10.1073/pnas.1207748109.
10. Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A., and Harmer, S. L. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130.Doi: 10.1186/gb-2008-9-8-r130.
11. Deckard, A., Anafi, R. C., Hogenesch, J. B., Haase, S. B., and Harer, J. (2013). Design and analysis oflarge-scalebiologicalrhythmstudies: acomparisonofalgorithms for detecting periodic signals in biological data. Bioinformatics 29, 3174-3180.Doi: 10.1093/bioinformatics/btt541.
12. De Lichtenberg, U., Jensen, L. J., Fausboll, A., Jensen, T. S., Bork, P., and Brunak, S. (2005). Comparison of computational methods for the identification of cell cycle-regulated genes. Bioinformatics 21, 1164-1171.Doi: 10.1093/bioinformatics/bti093.
13. Drechsel, G., Kahles, A., Kesarwani, A. K., Stauffer, E., Behr, J., Drewe, P., et al. (2013). Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome. Plant Cell 25, 3726-3742.Doi: 10.1105/tpc.113. 115485.
14. Dunlap, J. C., Loros, J. J., and Decoursey, P. J. (2004). Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer Associates.
15. Edwards, K. D., Anderson, P. E., Hall, A., Salathia, N. S., Locke, J. C., Lynn, J. R., et al. (2006). FLOWERING LOCUS C mediates natural variation in the high-temperatureresponseoftheArabidopsiscircadianclock. PlantCell 18,639-650.Doi: 10.1105/tpc.105.038315.
16. Farre, E. M., Harmer, S. L., Harmon, F. G., Yanovsky, M. J., and Kay, S. A. (2005). Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15,47-54.Doi: 10.1016/j.cub.2004.12.067.
17. Filichkin, S. A., Cumbie, J. S., Dharmawardhana, P., Jaiswal, P., Chang, J. H., Palusa, S. G., et al. (2015). Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Mol. Plant 8, 207-227.Doi: 10.1016/j.molp.2014.10.011.
18. Filichkin, S. A., and Mockler, T. C. (2012). Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biol. Direct. 7, 20.
19. Floris, M., Mahgoub, H., Lanet, E., Robaglia, C., and Menand, B. (2009). Post-transcriptional regulation of gene expression in plants during abiotic stress. Int. J. Mol. Sci. 10,3168-3185.Doi: 10.3390/ijms10073168.
20. Fujiwara, S., Wang, L., Han, L., Suh, S.S., Salome, P.A., Mcclung, C.R., et al.(2008). Post-translationalregulationoftheArabidopsiscircadianclockthroughselective proteolysis and phosphorylation of pseudo-response regulator proteins. J. Biol. Chem. 283, 23073-23083.Doi: 10.1074/jbc.M803471200.
21. Fustin, J. M., Doi, M., Yamaguchi, Y., Hida, H., Nishimura, S., Yoshida, M., et al. (2013). RNA-methylation-dependent RNA processing controls the speed ofthe circadian clock. Cell 155,793-806.Doi: 10.1016/j.cell.2013.10.026.
22. Gallie, D. R. (1993). Posttranscriptional regulation of gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 77-105.Doi: 10.1146/annurev.pp.44.060193.000453.
23. Grunwald, D., Singer, R. H., and Rout, M. (2011). Nuclear export dynamics of RNA-protein complexes. Nature 475, 333-341.Doi: 10.1038/nature10318.
24. Hamid, S. M., and Akgul, B. (2014). Master regulators of posttranscriptional gene expression are subject to regulation. Methods Mol. Biol. 1107, 303-310.Doi: 10.1007/978-1-62703-748-8_18.
25. Harmer, S. L., Hogenesch, J. B., Straume, M., Chang, H. S., Han, B., Zhu, T., et al. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.Doi: 10.1126/science.290.5499.2110.
26. Hazen, S. P., Naef, F., Quisel, T., Gendron, J. M., Chen, H., Ecker, J. R., et al. (2009).Exploringthetranscriptionallandscapeofplantcircadianrhythmsusing genome tiling arrays. Genome Biol. 10, R17.Doi: 10.1186/gb-2009-10-2-r17.
27. Hemmes, H., Henriques, R., Jang, I. C., Kim, S., and Chua, N. H. (2012). Circadian clock regulates dynamic chromatin modifications associated with Arabidopsis CCA1/LHY and TOC1 transcriptional rhythms. Plant Cell Physiol. 53, 2016-2029.Doi: 10.1093/pcp/pcs148.
28. Henriques, R., and Mas, P. (2013). Chromatin remodeling and alternative splicing: pre-and post-transcriptional regulation of the Arabidopsis circadian clock. Semin. Cell Dev. Biol. 24, 399-406.Doi: 10.1016/j.semcdb.2013.02.009.
29. Higgins, J. A., Bailey, P. C., and Laurie, D. A. (2010). Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5:e10065.Doi: 10.1371/journal.pone.0010065.
30. Hong, S., Song, H. R., Lutz, K., Kerstetter, R. A., Michael, T. P., and McClung, C. R. (2010). Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107,21211-21216.Doi: 10.1073/pnas.1011987107.
31. Hsu, P. Y., Devisetty, U. K., and Harmer, S. L. (2013). Accurate timekeeping is controlled by a cycling activator in Arabidopsis. Elife 2, e00473.Doi: 10.7554/eLife.00473.
32. Hsu, P. Y., and Harmer, S. L. (2012). Circadian phase has profound effects on differential expression analysis. PLoS ONE 7:e49853.Doi: 10.1371/journal.pone.0049853.
33. Huang, W., Perez-Garcia, P., Pokhilko, A., Millar, A. J., Antoshechkin, I., Riechmann, J. L., et al. (2012). Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75-79.Doi: 10.1126/science.1219075.
34. Hughes, M. E., Grant, G. R., Paquin, C., Qian, J., and Nitabach, M. N. (2012). Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. GenomeRes. 22,1266-1281.Doi: 10.1101/gr.128876.111.
35. Hughes, M.E., Hogenesch, J.B., and Kornacker, K.(2010).JTK_CYCLE:anefficient nonparametric algorithm for detecting rhythmic components in genome-scale datasets. J. Biol. Rhythms 25,372-380.Doi: 10.1177/0748730410379711.
36. Iwamoto, M., Higo, H., and Higo, K. (2000). Differential diurnal expression ofrice catalase genes: the 5' flanking region of CatA is not sufficient for circadian control. PlantSci. 151,39-46.
37. James, A. B., Syed, N. H., Bordage, S., Marshall, J., Nimmo, G. A., Jenkins, G. I., et al. (2012a). Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24, 961-981.Doi: 10.1105/tpc.111.093948.
38. James, A.B., Syed, N. H., Brown, J. W., and Nimmo, H. G. (2012b). Thermoplasticity in the plant circadian clock: how plants tell the time-perature. Plant Signal. Behav. 7,1219-1223.Doi: 10.4161/psb.21491.
39. Jones, M. A., Williams, B. A., Mcnicol, J., Simpson, C. G., Brown, J. W., and Harmer, S. L. (2012). Mutation of Arabidopsis spliceosomal timekeeper locus1 causes circadian clock defects. Plant Cell 24, 4066-4082.Doi: 10.1105/tpc.112.104828.
40. Jouannet, V, and Crespi, C. (2011). "9.4.1. Implications of npcRNAs in circadian cycle," in Long Non-Coding RNAs, ed. D. Ugarkovic (Berlin: Springer), 190-191.
41. Juntawong, P., and Bailey-Serres, J. (2012). Dynamic light regulation of translation status in Arabidopsis thaliana. Front. Plant Sci. 3:66.Doi: 10.3389/fpls.2012.00066.
42. Kadener, S., Menet, J. S., Sugino, K., Horwich, M. D., Weissbein, U., Nawathean, P., et al. (2009). A role for microRNAs in the Drosophila circadian clock. Genes Dev. 23,2179-2191.Doi: 10.1101/gad.1819509.
43. Kalyna, M., Simpson, C. G., Syed, N. H., Lewandowska, D., Marquez, Y., Kusenda, B., et al. (2012). Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res. 40, 2454-2469.Doi: 10.1093/nar/gkr932.
44. Kim, J. Y., Song, H. R., Taylor, B. L., and Carre, I. A. (2003). Light-regulated translation mediates gated induction of the Arabidopsis clock protein LHY. EMBO J. 22, 935-944.Doi: 10.1093/emboj/cdg075.
45. Koike, N., Yoo, S. H., Huang, H. C., Kumar, V., Lee, C., Kim, T. K., et al. (2012). Transcriptional architecture and chromatin landscape ofthe core circadian clock in mammals. Science 338, 349-354.Doi: 10.1126/science.1226339.
46. Kojima, S., Sher-Chen, E. L., and Green, C. B. (2012). Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 26, 2724-2736.Doi: 10.1101/gad.208306.112.
47. Kojima, S., Shingle, D. L., and Green, C. B. (2011). Post-transcriptional control of circadianrhythms. J. CellSci. 124,311-320.Doi: 10.1242/jcs.065771.
48. Kornblihtt, A. R., Schor, I. E., Allo, M., Dujardin, G., Petrillo, E., and Munoz, M. J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. CellBiol. 14,153-165.Doi: 10.1038/nrm3525.
49. Kwon, Y. J., Park, M. J., Kim, S. G., Baldwin, I. T., and Park, C. M. (2014). Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant Biol. 14:136.Doi: 10.1186/1471-2229-14-136.
50. Larrondo, L. F., Olivares-Yanez, C., Baker, C. L., Loros, J. J., and Dunlap, J. C. (2015). Circadianrhythms. Decouplingcircadianclockproteinturnoverfromcircadian period determination. Science 347, 1257-277.Doi: 10.1126/science.1257277.
51. Lee, H. G., Lee, K., Jang, K., and Seo, P. J. (2015). Circadian expression profiles of chromatin remodeling factor genes in Arabidopsis. J. Plant Res. 128, 187-199.Doi: 10.1007/s10265-014-0665-8.
52. Li, J., Grant, G. R., Hogenesch, J. B., and Hughes, M. E. (2015). Considerations for RNA-seq analysis of circadian rhythms. Methods Enzymol. 551, 349-367.Doi: 10.1016/bs.mie.2014.10.020.
53. Lidder, P., Gutierrez, R. A., Salome, P. A., Mcclung, C. R., and Green, P. J. (2005). Circadian control of messenger RNA stability. Association with a sequence-specific messenger RNA decay pathway. Plant Physiol. 138, 2374-2385.Doi: 10.1104/pp.105.060368.
54. Liu, M. J., Wu, S. H., and Chen, H. M. (2012). Widespread translational control contributes to the regulation ofArabidopsis photomorphogenesis. Mol. Syst. Biol. 8, 566.Doi: 10.1038/msb.2011.97.
55. Liu, Y., Hu, W., Murakawa, Y., Yin, J., Wang, G., Landthaler, M., et al. (2013). Cold-induced RNA-bindingproteinsregulatecircadiangeneexpressionbycontrolling alternative polyadenylation. Sci. Rep. 3, 2054.Doi: 10.1038/srep02054.
56. Lomb, N. (1976). Least-squares frequency analysis of unequally spaced data. Astrophys. Space Sci. 39, 447-462.
57. MacGregor, D. R., Gould, P., Foreman, J., Griffiths, J., Bird, S., Page, R., et al.(2013). HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES1 is required for circadian periodicity through the promotion of nucleo-cytoplasmic mRNA export in Arabidopsis. Plant Cell 25, 4391-4404.Doi: 10.1105/tpc.113.114959.
58. Malapeira, J., Khaitova, L. C., and Mas, P. (2012). Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc. Natl. Acad. Sci. U.S.A. 109,21540-21545.Doi: 10.1073/pnas.1217022110.
59. Mas, P., Kim, W. Y., Somers, D. E., and Kay, S. A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570.Doi: 10.1038/nature02163.
60. Matlin, A. J., Clark, F., and Smith, C. W. (2005). Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 6, 386-398.Doi: 10.1038/nrm1645.
61. McClung, C. R. (2014). Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Rep. 6, 2.Doi: 10.12703/P6-2.
62. McNeil, G. P., Zhang, X., Genova, G., and Jackson, F. R. (1998). A molecular rhythm mediating circadian clock output in Drosophila. Neuron 20, 297-303.
63. Meeks, L. R., Addepalli, B., and Hunt, A. G. (2009). Characterization of genes encodingpoly(A)polymerasesinplants:evidenceforduplicationandfunctional specialization. PLoS ONE 4:e8082.Doi: 10.1371/journal.pone.0008082.
64. Menet, J. S., Rodriguez, J., Abruzzi, K. C., and Rosbash, M. (2012). Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. Elife 1, e00011.Doi: 10.7554/eLife.00011.
65. Merkle, T. (2011). Nucleo-cytoplasmic transport of proteins and RNA in plants. PlantCellRep. 30,153-176.Doi: 10.1007/s00299-010-0928-3.
66. Millar, A. J., and Kay, S. A. (1991). Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell 3, 541-550.Doi: 10.1105/tpc.3.5.541.
67. Missra, A., and von Arnim, A. G. (2014). Analysis of mRNA translation states in Arabidopsis over the diurnal cycle by polysome microarray. Methods Mol. Biol. 1158,157-174.Doi: 10.1007/978-1-4939-0700-7_10.
68. Mockler, T. C., Michael, T. P., Priest, H. D., Shen, R., Sullivan, C. M., Givan, S. A., et al. (2007). The DIURNAL project: diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold. SpringHarb. Symp. Quant. Biol. 72, 353-363.Doi: 10.1101/sqb.2007.72.006.
69. Murakami, M., Tago, Y., Yamashino, T., and Mizuno, T. (2007). Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. PlantCellPhysiol. 48,110-121.Doi: 10.1093/pcp/pcl043.
70. Nagel, D. H., and Kay, S. A. (2012). Complexityinthewiringandregulationofplant circadian networks. Curr. Biol. 22, R648-R657.Doi: 10.1016/j.cub.2012.07.025.
71. Nakamichi, N., Kiba, T., Kamioka, M., Suzuki, T., Yamashino, T., Higashiyama, T., et al. (2012). Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc. Natl. Acad. Sci. U.S.A. 109, 17123-17128.Doi: 10.1073/pnas.1205156109.
72. Nicholson, P., Yepiskoposyan, H., Metze, S., Zamudio Orozco, R., Kleinschmidt, N., and Muhlemann, O. (2010). Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond qualitycontrol and the double-life of NMD factors. Cell. Mol. Life Sci. 67, 677-700.Doi: 10.1007/s00018-009-0177-1.
73. Nilsen, T. W., and Graveley, B. R. (2010). Expansion ofthe eukaryotic proteome by alternative splicing. Nature 463, 457-463.Doi: 10.1038/nature08909.
74. Parry, G. (2014). Components of the Arabidopsis nuclear pore complex play multiple diverse roles in control of plant growth. J. Exp. Bot. 65, 6057-6067.Doi: 10.1093/jxb/eru346.
75. Parry, G. (2015). The plant nuclear envelope and regulation of gene expression. J. Exp. Bot. 66,1673-1685.Doi: 10.1093/jxb/erv023.
76. Perez-Santangelo, S., Mancini, E., Francey, L. J., Schlaen, R. G., Chernomoretz, A., Hogenesch, J. B., et al. (2014). Role for LSM genes in the regulation of circadian rhythms. Proc. Natl. Acad. Sci. U.S.A. 111, 15166-15171.Doi: 10.1073/pnas.1409791111.
77. Perez-Santangelo, S., Schlaen, R. G., and Yanovsky, M. J. (2013). Genomic analysis reveals novel connections between alternative splicing and circadian regulatory networks. BriefFunct. Genomics 12, 13-24.Doi: 10.1093/bfgp/els052.
78. Pilgrim, M. L., Caspar, T., Quail, P. H., and Mcclung, C. R. (1993). Circadian and light-regulated expressionofnitrate reductase in Arabidopsis. PlantMol. Biol. 23, 349-364.
79. Reddy, A. S., Marquez, Y., Kalyna, M., and Barta, A. (2013). Complexity of the alternative splicing landscape in plants. Plant Cell 25, 3657-3683.Doi: 10.1105/tpc.113.117523.
80. Riehs-Kearnan, N., Gloggnitzer, J., Dekrout, B., Jonak, C., and Riha, K. (2012). Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. Nucleic Acids Res. 40, 5615-5624.Doi: 10.1093/nar/gks195.
81. Robinson, B. G., Frim, D. M., Schwartz, W. J., and Majzoub, J. A. (1988). Vasopressin mRNA in the suprachiasmatic nuclei: daily regulation of polyadenylate tail length. Science 241, 342-344.
82. Rodriguez, J., Tang, C. H., Khodor, Y. L., Vodala, S., Menet, J. S., and Rosbash, M. (2013). Nascent-Seq analysis of Drosophila cycling gene expression. Proc. Natl. Acad. Sci. U.S.A. 110,E275-E284.Doi: 10.1073/pnas.1219969110.
83. Romanowski, A., Garavaglia, M. J., Goya, M. E., Ghiringhelli, P. D., and Golombek, D. A. (2014). Potential conservation of circadian clock proteins in the phylum Nematoda as revealed by bioinformatic searches. PLoS ONE 9:e112871.Doi: 10.1371/journal.pone.0112871.
84. Rugnone, M. L., Faigon Soverna, A., Sanchez, S. E., Schlaen, R. G., Hernando, C. E. , Seymour, D. K., et al. (2013). LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc. Natl. Acad. Sci. U.S.A. 110,12120-12125.Doi: 10.1073/pnas.1302170110.
85. Sanchez, S. E., Petrillo, E., Beckwith, E. J., Zhang, X., Rugnone, M. L., Hernando, C. E., et al. (2010). A methyl transferase links the circadian clock to the regulation ofalternative splicing. Nature 468, 112-116.Doi: 10.1038/nature09470.
86. Sanchez, S. E., and Yanovsky, M. J. (2013). Time for a change. Elife 2, e00791.Doi: 10.7554/eLife.00791.
87. Scargle, J. (1982). Studies in astronomical time series analysis. II-Statistical aspects ofspectralanalysis ofunevenlyspaced data. Astrophys. J. 263, 835-853.
88. Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M., and Wisman, E. (2001). Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. PlantCell 13,113-123.Doi: 10.1105/tpc.13.1.113.
89. Schoning, J. C., Streitner, C., Meyer, I. M., Gao, Y., and Staiger, D. (2008). Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res. 36, 6977-6987.Doi: 10.1093/nar/gkn847.
90. Schoning, J. C., Streitner, C., Page, D. R., Hennig, S., Uchida, K., Wolf, E., et al. (2007). Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J. 52, 1119-1130.Doi: 10.1111/j.1365-313X.2007. 03302.x.
91. Seo, P. J., and Mas, P. (2014). Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26, 79-87.Doi: 10.1105/tpc.113.119842.
92. Seo, P. J., Park, M. J., Lim, M. H., Kim, S. G., Lee, M., Baldwin, I. T., et al. (2012). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24, 2427-2442.Doi: 10.1105/tpc.112.098723.
93. Sire, C., Moreno, A. B., Garcia-Chapa, M., Lopez-Moya, J. J., and San Segundo, B. (2009). Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS Lett. 583, 1039-1044.Doi: 10.1016/j.febslet.2009.02.024.
94. Song, Y. H., Ito, S., and Imaizumi, T. (2010). Similarities in the circadian clock and photoperiodism in plants. Curr. Opin. Plant Biol. 13, 594-603.Doi: 10.1016/j.pbi.2010.05.004.
95. Staiger, D. (2001). RNA-binding proteins and circadian rhythms in Arabidopsis thaliana. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1755-1759.Doi: 10.1098/rstb.2001.0964.
96. Straume, M. (2004). DNA microarray time series analysis: automated statistical assessment of circadian rhythms in gene expression patterning. Methods Enzymol. 383, 149-166.Doi: 10.1016/S0076-6879(04)83007-6.
97. Suzuki, Y., Arae, T., Green, P. J., Yamaguchi, J., and Chiba, Y. (2015). AtCCR4a and AtCCR4b are involved in determining the poly(A) length ofgranule-bound starch synthase 1 transcript and modulating sucrose and starch metabolism in Arabidopsis thaliana. Plant Cell Physiol.Doi: 10.1093/pcp/pcv012.
98. Syed, N. H., Kalyna, M., Marquez, Y., Barta, A., and Brown, J. W. (2012). Alternative splicing in plants-coming ofage. Trends Plant Sci. 17, 616-623.Doi: 10.1016/j.tplants.2012.06.001.
99. Wahl, M. C., Will, C. L., and Luhrmann, R. (2009). The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718.Doi: 10.1016/j.cell.2009.02.009.
100. Waltenberger, H., Schneid, C., Grosch, J. O., Bareiss, A., and Mittag, M. (2001). Identification of target mRNAs for the clock-controlled RNA-binding protein Chlamy1 fromChlamydomonasreinhardtii. Mol. Genet. Genomics 265,180-188.
101. Wang, H., Chung, P. J., Liu, J., Jang, I. C., Kean, M. J., Xu, J., et al. (2014). Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res. 24, 444-453.Doi: 10.1101/gr.165555.113.
102. Wang, X., Wu, F., Xie, Q., Wang, H., Wang, Y., Yue, Y., et al. (2012). SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24, 3278-3295.Doi: 10.1105/tpc.112.100081.
103. Wichert, S., Fokianos, K., and Strimmer, K. (2004). Identifying periodically expressed transcripts in microarray time series data. Bioinformatics 20, 5-20.Doi: 10.1093/bioinformatics/btg364.
104. Wu, G., Zhu, J., Yu, J., Zhou, L., Huang, J. Z., and Zhang, Z. (2014). Evaluation of five methods for genome-wide circadian gene identification. J. Biol. Rhythms 29, 231-242.Doi: 10.1177/0748730414537788.
105. Xie, Q., Wang, P., Liu, X., Yuan, L., Wang, L., Zhang, C., et al. (2014). LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26, 2843-2857.Doi: 10.1105/tpc.114.126573.
106. Yakir, E., Hilman, D., Hassidim, M., and Green, R. M. (2007). CIRCADIAN CLOCK ASSOCIATED1 transcript stability and the entrainment of the circadian clockin Arabidopsis. Plant Physiol. 145, 925-932.Doi: 10.1104/pp.107.103812.
107. Yang, R., and Su, Z. (2010). Analyzing circadian expression data by harmonic regression based on autoregressive spectral estimation. Bioinformatics 26, i168-i174.Doi: 10.1093/bioinformatics/btq189.
108. Yoshitane, H., Ozaki, H., Terajima, H., Du, N. H., Suzuki, Y., Fujimori, T., et al. (2014). CLOCK-controlled polyphonic regulation of circadian rhythms through canonical and noncanonical E-boxes. Mol. Cell. Biol. 34, 1776-1787.Doi: 10.1128/MCB.01465-13.
109. Zhao, B., Schneid, C., Iliev, D., Schmidt, E. M., Wagner, V., Wollnik, F., et al. (2004). The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology domain-containing subunits. Eukaryot. Cell 3,815-825.Doi: 10.1128/EC.3.3.815-825.2004.
110. Zhong, H. H., Resnick, A. S., Straume, M., and Robertson Mcclung, C. (1997). Effects of synergistic signaling by phytochrome A and cryptochrome1 on circadian clock-regulated catalase expression. Plant Cell 9, 947-955.
111. Ziemienowicz, A., Haasen, D., Staiger, D., and Merkle, T. (2003). Arabidopsis transportin1 is the nuclear import receptor for the circadian clock-regulated RNA-binding protein AtGRP7. Plant Mol. Biol. 53, 201-212.Doi: 10.1023/B:PLAN.0000009288.46713.1f.