Genomic analysis reveals novel connections between alternative splicing and circadian regulatory networks

Briefings in Functional Genomics

Volumn 12, Issue 1, 2013, Pages 13-24

  Perez santángelo, Soledad ^a   Schlaen, Rubén Gustavo ^a   Yanovsky, Marcelo J ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Alternative splicing; Arabidopsis thaliana; Circadian rhythms; Gene expression networks

Indexed keywords

GLYCINE RICH PROTEIN 7; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ABIOTIC STRESS; ALTERNATIVE RNA SPLICING; ARABIDOPSIS; ARTICLE; BEHAVIOR; CIRCADIAN RHYTHM; DROSOPHILA; ENVIRONMENTAL CHANGE; EXON; GENE EXPRESSION; GENE MUTATION; GENETIC SELECTION; GENETIC TRANSCRIPTION; GENOMICS; HIGH THROUGHPUT SEQUENCING; INTRON RETENTION; LIGHT; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA SEQUENCE; SIGNAL TRANSDUCTION; TEMPERATURE;

ALTERNATIVE SPLICING; ANIMALS; CIRCADIAN CLOCKS; GENE REGULATORY NETWORKS; GENOMICS; HUMANS; PLANTS; SIGNAL TRANSDUCTION;

ARABIDOPSIS THALIANA; EUKARYOTA; PROKARYOTA;

EID: 84872815534     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els052     Document Type: Article

References (87)

1. Kalsotra A, Cooper TA. Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 2011;12:715-29.
2. Blencowe BJ. Alternative splicing: new insights from global analyses. Cell 2006;126:37-47.
3. Kalyna M, Simpson CG, Syed NH, et al. Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res 2012;40:2454-69.
4. Lewis BP, Green RE, Brenner SE. Evidence for the widespread coupling of alternative splicing and nonsensemediated mRNA decay in humans. Proc Natl Acad Sci USA 2003;100:189-92.
5. Salomonis N, Schlieve CR, Pereira L, et al. Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc Natl Acad Sci USA 2010;107:10514-9.
6. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010;463:457-63.
7. Stamm S, Ben-Ari S, Rafalska I, et al. Function of alternative splicing. Gene 2005;344:1-20.
8. Irimia M, Blencowe BJ. Alternative splicing: decoding an expansive regulatory layer. Curr Opin Cell Biol 2012;24:323-32.
9. Pan Q, Shai O, Lee LJ, et al. Deep surveying of alternative splicing complexity in the human transcriptome by highthroughput sequencing. Nat Genet 2008;40:1413-5.
10. Wang ET, Sandberg R, Luo S, et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008; 456:470-6.
11. Filichkin SA, Priest HD, Givan SA, et al. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 2010;20:45-58.
12. Marquez Y, Brown JW, Simpson C, et al. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 2012;22:1184-95.
13. Sanchez SE, Petrillo E, Kornblihtt AR, et al. Alternative splicing at the right time. RNA Biol 2011;8:954-9.
14. Staiger D, Green R. RNA-based regulation in the plant circadian clock. Trends Plant Sci 2011;16:517-23.
15. Kojima S, Shingle DL, Green CB. Post-transcriptional control of circadian rhythms. JCell Sci 2011;124:311-20.
16. Young MW, Kay SA. Time zones: a comparative genetics of circadian clocks. Nat RevGenet 2001;2:702-15.
17. Rosbash M. The implications of multiple circadian clock origins. PLoS Biol 2009;7:e62.
18. Alabadi D, Oyama T, Yanovsky MJ, et al. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 2001;293:880-3.
19. Farre EM, Harmer SL, Harmon FG, et al. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol 2005;15:47-54.
20. Nakamichi N, Kita M, Ito S, et al. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 2005;46:686-98.
21. Huang W, Perez-Garcia P, Pokhilko A, et al. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 2012;336:75-9.
22. Pokhilko A, Fernandez AP, Edwards KD, et al. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 2012;8:574.
23. Gendron JM, Pruneda-Paz JL, Doherty CJ, et al. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci USA 2012;109: 3167-72.
24. Rawat R, Takahashi N, Hsu PY, et al. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet 2011;7:e1001350.
25. Rawat R, Schwartz J, Jones MA, et al. REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 2009; 106:16883-8.
26. Farinas B, Mas P. Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. Plant J 2011;66:318-29.
27. Nusinow DA, Helfer A, Hamilton EE, et al. The ELF4- ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 2011;475:398-402.
28. Helfer A, Nusinow DA, Chow BY, et al. LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 2011;21:126-33.
29. Dixon LE, Knox K, Kozma-Bognar L, et al. Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Curr Biol 2011; 21:120-5.
30. Herrero E, Kolmos E, Bujdoso N, et al. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 2012;24:428-43.
31. Zheng X, Sehgal A. Speed control: cogs and gears that drive the circadian clock. Trends Neurosci 2012;35:574-85.
32. Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 2012;74:246-60.
33. Baker CL, Loros JJ, Dunlap JC. The circadian clock of Neurospora crassa. FEMS Microbiol Rev 2012;36:95-110.
34. Nakajima M, Imai K, Ito H, et al. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 2005;308:414-5.
35. Tomita J, Nakajima M, Kondo T, et al. No transcriptiontranslation feedback in circadian rhythm of KaiC phosphorylation. Science 2005;307:251-4.
36. Edgar RS, Green EW, Zhao Y, et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 2012;485: 459-64.
37. O'Neill JS, van Ooijen G, Dixon LE, et al. Circadian rhythms persist without transcription in a eukaryote. Nature 2011;469:554-8.
38. O'Neill JS, Reddy AB. Circadian clocks in human red blood cells. Nature 2011;469:498-503.
39. Brown SA, Kowalska E, Dallmann R. (Re)inventing the circadian feedback loop. Dev Cell 2012;22:477-487.
40. Gallego M, Virshup DM. Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 2007;8:139-48.
41. Farre EM, Weise SE. The interactions between the circadian clock and primary metabolism. Curr Opin Plant Biol 2012;15:293-300.
42. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science 2010;330:1349-54.
43. Eckel-Mahan K, Sassone-Corsi P. Metabolism control by the circadian clock and vice versa. Nat StructMol Biol 2009; 16:462-7.
44. Staiger D, Koster T. Spotlight on post-transcriptional control in the circadian system. Cell Mol Life Sci 2011;68:71-83.
45. Zhang L, Weng W, Guo J. Posttranscriptional mechanisms in controlling eukaryotic circadian rhythms. FEBS Lett 2011;585:1400-5.
46. Citri Y, Colot HV, Jacquier AC, et al. A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature 1987;326:42-7.
47. Cheng Y, Gvakharia B, Hardin PE. Two alternatively spliced transcripts from the Drosophila period gene rescue rhythms having different molecular and behavioral characteristics. Mol Cell Biol 1998;18:6505-14.
48. Colot HV, Loros JJ, Dunlap JC. Temperature-modulated alternative splicing and promoter use in the Circadian clock gene frequency. Mol Biol Cell 2005;16:5563-71.
49. Diernfellner AC, Schafmeier T, Merrow MW, et al. Molecular mechanism of temperature sensing by the circadian clock of Neurospora crassa. Genes Dev 2005;19:1968-73.
50. Sanchez SE, Petrillo E, Beckwith EJ, et al. A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 2010;468:112-6.
51. James AB, Syed NH, Bordage S, et al. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 2012;24:961-81.
52. Filichkin SA, Mockler TC. Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biol Direct 2012;7:20.
53. Majercak J, Sidote D, Hardin PE, et al. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 1999;24:219-230.
54. Collins BH, Rosato E, Kyriacou CP. Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 2004;101:1945-50.
55. Majercak J, Chen WF, Edery I. Splicing of the period gene 30-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 2004;24:3359-72.
56. Chen WF, Low KH, Lim C, et al. Thermosensitive splicing of a clock gene and seasonal adaptation. Cold Spring Harb Symp Quant Biol 2007;72:599-606.
57. Low KH, Lim C, Ko HW, et al. Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 2008;60:1054-67.
58. Diernfellner A, Colot HV, Dintsis O, et al. Long and short isoforms of Neurospora clock protein FRQ support temperature-compensated circadian rhythms. FEBS Lett 2007;581:5759-5764.
59. Wang X, Wu F, Xie Q, et al. SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 2012;24:3278-95.
60. Seo PJ, Park MJ, Lim MH, et al. A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 2012;24:2427-42.
61. Carpenter CD, Kreps JA, Simon AE. Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol 1994;104:1015-25.
62. Heintzen C, Melzer S, Fischer R, et al. A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. PlantJ 1994; 5:799-813.
63. Streitner C, Danisman S, Wehrle F, et al. The small glycinerich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. PlantJ 2008;56:239-50.
64. Kim JS, Jung HJ, Lee HJ, et al. Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 2008;55:455-66.
65. Schoning JC, Streitner C, Meyer IM, et al. 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 2008;36:6977-87.
66. Staiger D, Zecca L, Wieczorek Kirk DA, et al. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 2003;33:361-71.
67. Zhang N, Kallis RP, Ewy RG, et al. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 2002;99:3330-4.
68. Hazen SP, Naef F, Quisel T, et al. Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol 2009;10:R17.
69. Hughes ME, Grant GR, Paquin C, et al. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res 2012;22:1266-81.
70. McGlincy NJ, Valomon A, Chesham JE, et al. Regulation of alternative splicing by the circadian clock and food related cues. Genome Biol 2012;13:R54.
71. Kula-Eversole E, Nagoshi E, Shang Y, et al. Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila. Proc Natl Acad Sci USA 2010;107:13497-502.
72. Wahl MC, Will CL, Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18.
73. Matlin AJ, Clark F, Smith CW. Understanding alternative splicing: towards a cellular code. NatRevMolCell Biol 2005; 6:386-98.
74. Graveley BR. Alternative splicing: regulation without regulators. Nat StructMol Biol 2009;16:13-5.
75. Luco RF, Allo M, Schor IE, et al. Epigenetics in alternative pre-mRNA splicing. Cell 2011;144:16-26.
76. Huang Y, Li W, Yao X, et al. Mediator complex regulates alternative mRNA processing via the MED23 subunit. Mol Cell 2012;45:459-69.
77. Luco RF, Pan Q, Tominaga K, et al. Regulation of alternative splicing by histone modifications. Science 2010;327: 996-1000.
78. Rosel TD, Hung LH, Medenbach J, et al. RNA-Seq analysis in mutant zebrafish reveals role of U1C protein in alternative splicing regulation. EMBOJ 2011;30:1965-76.
79. Saltzman AL, Pan Q, Blencowe BJ. Regulation of alternative splicing by the core spliceosomal machinery. GenesDev 2011;25:373-84.
80. Zhang Z, Lotti F, Dittmar K, et al. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 2008;133: 585-600.
81. Shikata H, Shibata M, Ushijima T, et al. The RS domain of Arabidopsis splicing factor RRC1 is required for phytochrome B signal transduction. Plant J 2012;70: 727-38.
82. Li W, Dai C, Liu CC, et al. Algorithm to identify frequent coupled modules from two-layered network series: application to study transcription and splicing coupling. J Comput Biol 2012;19:710-30.
83. Faure S, Turner AS, Gruszka D, et al. Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. ProcNatl Acad SciUSA 2012;109:8328-33.
84. Zakhrabekova S, Gough SP, Braumann I, et al. Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. ProcNatl Acad Sci USA 2012;109:4326-31.
85. Turner A, Beales J, Faure S, et al. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 2005;310:1031-4.
86. Murphy RL, Klein RR, Morishige DT, et al. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci USA 2011;108:16469-74.
87. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009;136:777-93.