Alternative splicing at the intersection of biological timing, development, and stress responses

Plant Cell

Volumn 25, Issue 10, 2013, Pages 3640-3656

  Staiger, Dorothee ^a,b   Brown, John W S ^c,d  

^a BIELEFELD UNIVERSITY   (Germany)

^b Institute for Genome Research and Systems Biology   (Germany)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT RNA; RNA BINDING PROTEIN; RNA PRECURSOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

ALTERNATIVE RNA SPLICING; CIRCADIAN RHYTHM; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DEVELOPMENT; SPLICEOSOME;

ALTERNATIVE SPLICING; CIRCADIAN CLOCKS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; PLANT DEVELOPMENT; PLANT PROTEINS; RNA PRECURSORS; RNA, PLANT; RNA-BINDING PROTEINS; SPLICEOSOMES; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84888396486     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.113803     Document Type: Review

References (170)

1. Agafonov, D.E., Deckert, J., Wolf, E., Odenwälder, P., Bessonov, S., Will, C.L., Urlaub, H., and Lührmann, R. (2011). Semiquantitative proteomic analysis of the human spliceosome via a novel twodimensional gel electrophoresis method. Mol. Cell. Biol. 31: 2667-2682.
2. Airoldi, C.A., and Davies, B. (2012). Gene duplication and the evolution of plant MADS-box transcription factors. J. Genet. Genomics 39: 157-165.
3. Ali, G.S., Golovkin, M., and Reddy, A.S. (2003). Nuclear localization and in vivo dynamics of a plant-specific serine/arginine-rich protein. Plant J. 36: 883-893.
4. Ali, G.S., Palusa, S.G., Golovkin, M., Prasad, J., Manley, J.L., and Reddy, A.S.N. (2007). Regulation of plant developmental processes by a novel splicing factor. PLoS ONE 2: e471.
5. Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13: 627-639.
6. Balasubramanian, S., Sureshkumar, S., Lempe, J., and Weigel, D. (2006). Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2: e106.
7. Balasubramanian, S., and Weigel, D. (2006). Temperature induced flowering in Arabidopsis thaliana. Plant Signal. Behav. 1: 227-228.
8. Berget, S.M., Moore, C., and Sharp, P.A. (1977). Spliced segments at the 59 terminus of adenovirus 2 late mRNA. Proc. Natl. Acad. Sci. USA 74: 3171-3175.
9. Bournay, A.-S., Hedley, P.E., Maddison, A., Waugh, R., and Machray, G.C. (1996). Exon skipping induced by cold stress in a potato invertase gene transcript. Nucleic Acids Res. 24: 2347-2351.
10. Bove, J., Kim, C.Y., Gibson, C.A., and Assmann, S.M. (2008). Characterization of wound-responsive RNA-binding proteins and their splice variants in Arabidopsis. Plant Mol. Biol. 67: 71-88.
11. Breeze, E., et al. (2011). High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23: 873-894.
12. Brown, J.W.S. (1996). Arabidopsis intron mutations and pre-mRNA splicing. Plant J. 10: 771-780.
13. Brummell, D.A., Chen, R.K.Y., Harris, J.C., Zhang, H., Hamiaux, C., Kralicek, A.V., and McKenzie, M.J. (2011). Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to coldinduced sweetening resistance and includes spliced hybrid mRNA variants. J. Exp. Bot. 62: 3519-3534.
14. Cai, X.-L., Wang, Z.-Y., Xing, Y.-Y., Zhang, J.-L., and Hong, M.-M. (1998). Aberrant splicing of intron 1 leads to the heterogeneous 59 UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. Plant J. 14: 459-465.
15. Cao, S., Jiang, L., Song, S., Jing, R., and Xu, G. (2006). AtGRP7 is involved in the regulation of abscisic acid and stress responses in Arabidopsis. Cell. Mol. Biol. Lett. 11: 526-535.
16. Carpenter, C.D., Kreps, J.A., and Simon, A.E. (1994). Genes encoding glycine-rich Arabidopsis thaliana proteins with RNAbinding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol. 104: 1015-1025.
17. Carvalho, R.F., Carvalho, S.D., and Duque, P. (2010). The plantspecific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol. 154: 772-783.
18. Christensen, A.H., Sharrock, R.A., and Quail, P.H. (1992). Maize polyubiquitin genes: Structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol. Biol. 18: 675-689.
19. Chung, H.S., Cooke, T.F., Depew, C.L., Patel, L.C., Ogawa, N., Kobayashi, Y., and Howe, G.A. (2010). Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling. Plant J. 63: 613-622.
20. Chung, T., Wang, D., Kim, C.S., Yadegari, R., and Larkins, B.A. (2009). Plant SMU-1 and SMU-2 homologues regulate pre-mRNA splicing and multiple aspects of development. Plant Physiol. 151: 1498-1512.
21. Darracq, A., and Adams, K.L. (2013). Features of evolutionarily conserved alternative splicing events between Brassica and Arabidopsis. New Phytol. 199: 252-263.
22. de la Fuente van Bentem, S., et al. (2008). Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis. J. Proteome Res. 7: 2458-2470.
23. Deng, X., Gu, L., Liu, C., Lu, T., Lu, F., Lu, Z., Cui, P., Pei, Y., Wang, B., Hu, S., and Cao, X. (2010). Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper premRNA splicing. Proc. Natl. Acad. Sci. USA 107: 19114-19119.
24. Dinesh-Kumar, S.P., and Baker, B.J. (2000). Alternatively spliced N resistance gene transcripts: Their possible role in tobacco mosaic virus resistance. Proc. Natl. Acad. Sci. USA 97: 1908-1913.
25. Filichkin, S.A., Priest, H.D., Givan, S.A., Shen, R., Bryant, D.W., Fox, S.E., Wong, W.K., and Mockler, T.C. (2010). Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res. 20: 45-58.
26. Fouquet, R., Martin, F., Fajardo, D.S., Gault, C.M., Gómez, E., Tseung, C.-W., Policht, T., Hueros, G., and Settles, A.M. (2011). Maize rough endosperm3 encodes an RNA splicing factor required for endosperm cell differentiation and has a nonautonomous effect on embryo development. Plant Cell 23: 4280-4297.
27. Gan, X., et al. (2011). Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423.
28. Golisz, A., Sikorski, P.J., Kruszka, K., and Kufel, J. (2013). Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation. Nucleic Acids Res. 41: 6232-6249.
29. Graveley, B.R. (2005). Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 123: 65-73.
30. Gross-Hardt, R., Kägi, C., Baumann, N., Moore, J.M., Baskar, R., Gagliano, W.B., Jürgens, G., and Grossniklaus, U. (2007). LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol. 5: e47.
31. Guan, Q., Wu, J., Zhang, Y., Jiang, C., Liu, R., Chai, C., and Zhu, J. (2013). A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25: 342-356.
32. Gulledge, A.A., Roberts, A.D., Vora, H., Patel, K., and Loraine, A.E. (2012). Mining Arabidopsis thaliana RNA-seq data with Integrated Genome Browser reveals stress-induced alternative splicing of the putative splicing regulator SR45a. Am. J. Bot. 99: 219-231.
33. Hackmann, C., Korneli, C., Kutyniok, M., Köster, T., Wiedenlübbert, M., Müller, C., and Staiger, D. (August 21, 2013). Salicylic acid-dependent and-independent impact of an RNA-binding protein on plant immunity. Plant Cell Environ., doi/10.1111/pce.12188.
34. Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kreps, J.A., and Kay, S.A. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
35. Hazen, S.P., Naef, F., Quisel, T., Gendron, J.M., Chen, H., Ecker, J.R., Borevitz, J.O., and Kay, S.A. (2009). Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol. 10: R17.
36. Herrero, E., and Davis, S.J. (2012). Time for a nuclear meeting: Protein trafficking and chromatin dynamics intersect in the plant circadian system. Mol. Plant 5: 554-565.
37. Hogg, R., McGrail, J.C., and O'Keefe, R.T. (2010). The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Biochem. Soc. Trans. 38: 1110-1115.
38. 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. USA 107: 21211-21216.
39. Hugouvieux, V., Kwak, J.M., and Schroeder, J.I. (2001). An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106: 477-487.
40. Iida, K., Seki, M., Sakurai, T., Satou, M., Akiyama, K., Toyoda, T., Konagaya, A., and Shinozaki, K. (2004). Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on fulllength cDNA sequences. Nucleic Acids Res. 32: 5096-5103.
41. International Barley Genome Sequencing Consortium (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711-716.
42. Isshiki, M., Morino, K., Nakajima, M., Okagaki, R.J., Wessler, S.R., Izawa, T., and Shimamoto, K. (1998). A naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 59 splice site of the first intron. Plant J. 15: 133-138.
43. James, A.B., Syed, N.H., Bordage, S., Marshall, J., Nimmo, G.A., Jenkins, G.I., Herzyk, P., Brown, J.W.S., and Nimmo, H.G. (2012b). Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24: 961-981.
44. James, A.B., Syed, N.H., Brown, J.W.S., and Nimmo, H.G. (2012a). Thermoplasticity in the plant circadian clock: How plants tell the time-perature. Plant Signal. Behav. 7: 1219-1223.
45. Jeong, B.R., Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., Yu, M., Cerny, R.L., Staiger, D., Alfano, J.R., and Xu, Y. (2011). Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem. 286: 43272-43281.
46. Jeong, H.-J., Kim, Y.J., Kim, S.H., Kim, Y.-H., Lee, I.-J., Kim, Y.K., and Shin, J.S. (2012). Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense. Plant Cell Physiol. 52: 2147-2156.
47. Jia, F., and Rock, C.D. (2013). MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Mol. Biol. 81: 447-460.
48. Jones, M.A., Williams, B.A., McNicol, J., Simpson, C.G., Brown, J.W.S., and Harmer, S.L. (2012). Mutation of Arabidopsis spliceosomal timekeeper locus1 causes circadian clock defects. Plant Cell 24: 4066-4082.
49. Kalyna, M., Lopato, S., and Barta, A. (2003). Ectopic expression of atRSZ33 reveals its function in splicing and causes pleiotropic changes in development. Mol. Biol. Cell 14: 3565-3577.
50. Kalyna, M., Lopato, S., Voronin, V., and Barta, A. (2006). Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins. Nucleic Acids Res. 34: 4395-4405.
51. Kalyna, M., et al. (2012). Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res. 40: 2454-2469.
52. Kaufmann, K., Muiño, J.M., Østerås, M., Farinelli, L., Krajewski, P., and Angenent, G.C. (2010). Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat. Protoc. 5: 457-472.
53. Kazan, K. (2003). Alternative splicing and proteome diversity in plants: The tip of the iceberg has just emerged. Trends Plant Sci. 8: 468-471.
54. Kesari, R., Lasky, J.R., Villamor, J.G., Des Marais, D.L., Chen, Y.-J.C., Liu, T.-W., Lin, W., Juenger, T.E., and Verslues, P.E. (2012). Intronmediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation. Proc. Natl. Acad. Sci. USA 109: 9197-9202.
55. Kim, J.S., Jung, H.J., Lee, H.J., Kim, K.A., Goh, C.H., Woo, Y., Oh, S.H., Han, Y.S., and Kang, H. (2008). Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J. 55: 455-466.
56. Kim, S.H., Kwon, S.I., Saha, D., Anyanwu, N.C., and Gassmann, W. (2009). Resistance to the Pseudomonas syringae Effector HopA1 Is Governed by the TIR-NBS-LRR Protein RPS6 and Is Enhanced by Mutations in SRFR1. Plant Physiol. 150: 1723-1732.
57. Koncz, C., Dejong, F., Villacorta, N., Szakonyi, D., and Koncz, Z. (2012). The spliceosome-activating complex: Molecular mechanisms underlying the function of a pleiotropic regulator. Front. Plant Sci. 3: 9.
58. Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., and Muñoz, M.J. (2013). Alternative splicing: A pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14: 153-165.
59. Koroleva, O.A., Calder, G., Pendle, A.F., Kim, S.H., Lewandowska, D., Simpson, C.G., Jones, I.M., Brown, J.W.S., and Shaw, P.J. (2009). Dynamic behavior of Arabidopsis eIF4A-III, putative core protein of exon junction complex: Fast relocation to nucleolus and splicing speckles under hypoxia. Plant Cell 21: 1592-1606.
60. Kramer, M., Boeck, J., Reichenbach, D., Kaether, C., Schreiber, S., Platzer, M., Rosenstiel, P., and Huse, K. (2010). NOD2-C2-a novel NOD2 isoform activating NF-kappaB in a muramyl dipeptideindependent manner. BMC Res. Notes 3: 224.
61. Kriechbaumer, V., Wang, P., Hawes, C., and Abell, B.M. (2012). Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation. Plant J. 70: 292-302.
62. Kumar, K.R., and Kirti, P.B. (2012). Novel role for a serine/argininerich splicing factor, AdRSZ21 in plant defense and HR-like cell death. Plant Mol. Biol. 80: 461-476.
63. Lambermon, M.H., Fu, Y., Wieczorek Kirk, D.A., Dupasquier, M., Filipowicz, W., and Lorkovic, Z.J. (2002). UBA1 and UBA2, two proteins that interact with UBP1, a multifunctional effector of premRNA maturation in plants. Mol. Cell. Biol. 22: 4346-4357.
64. Lambermon, M.H., Simpson, G.G., Wieczorek Kirk, D.A., Hemmings-Mieszczak, M., Klahre, U., and Filipowicz, W. (2000). UBP1, a novel hnRNP-like protein that functions at multiple steps of higher plant nuclear pre-mRNA maturation. EMBO J. 19: 1638-1649.
65. Larkin, P.D., and Park, W.D. (1999). Transcript accumulation and utilization of alternate and non-consensus splice sites in rice granule-bound starch synthase are temperature-sensitive and controlled by a single-nucleotide polymorphism. Plant Mol. Biol. 40: 719-727.
66. Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J.U., Rätsch, G., and Weigel, D. (2008). Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105: 8795-8800.
67. Lazar, G., and Goodman, H.M. (2000). The Arabidopsis splicing factor SR1 is regulated by alternative splicing. Plant Mol. Biol. 42: 571-581.
68. Lee, B.H., Kapoor, A., Zhu, J., and Zhu, J.K. (2006). STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18: 1736-1749.
69. Li, J., Kinoshita, T., Pandey, S., Ng, C.K., Gygi, S.P., Shimazaki, K., and Assmann, S.M. (2002). Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 418: 793-797.
70. Lim, G.-H., Zhang, X., Chung, M.-S., Lee, D.J., Woo, Y.-M., Cheong, H.-S., and Kim, C.S. (2010). A putative novel transcription factor, AtSKIP, is involved in abscisic acid signalling and confers salt and osmotic tolerance in Arabidopsis. New Phytol. 185: 103-113.
71. Liu, J., Sun, N., Liu, M., Liu, J., Du, B., Wang, X., and Qi, X. (2013). An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol. 162: 512-521.
72. Liu, M., Yuan, L., Liu, N.Y., Shi, D.Q., Liu, J., and Yang, W.C. (2009). GAMETOPHYTIC FACTOR 1, involved in pre-mRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J. Integr. Plant Biol. 51: 261-271.
73. Lopato, S., Kalyna, M., Dorner, S., Kobayashi, R., Krainer, A.R., and Barta, A. (1999). atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev. 13: 987-1001.
74. Lu, T., Lu, G., Fan, D., Zhu, C., Li, W., Zhao, Q., Feng, Q., Zhao, Y., Guo, Y., Li, W., Huang, X., and Han, B. (2010). Function annotation of the rice transcriptome at single-nucleotide resolution by RNAseq. Genome Res. 20: 1238-1249.
75. Luco, R.F., Allo, M., Schor, I.E., Kornblihtt, A.R., and Misteli, T. (2011). Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26.
76. Marone, D., Russo, M.A., Laidò, G., De Leonardis, A.M., and Mastrangelo, A.M. (2013). Plant nucleotide binding site-leucinerich repeat (NBS-LRR) genes: Active guardians in host defense responses. Int. J. Mol. Sci. 14: 7302-7326.
77. Marquez, Y., Brown, J.W.S., Simpson, C.G., Barta, A., and Kalyna, M. (2012). Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res. 22: 1184-1195.
78. Más, P. (2008). Circadian clock function in Arabidopsis thaliana: Time beyond transcription. Trends Cell Biol. 18: 273-281.
79. Mastrangelo, A.M., Marone, D., Laidò, G., De Leonardis, A.M., and De Vita, P. (2012). Alternative splicing: Enhancing ability to cope with stress via transcriptome plasticity. Plant Sci. 185-186: 40-49.
80. Matlin, A.J., Clark, F., and Smith, C.W.J. (2005). Understanding alternative splicing: Towards a cellular code. Nat. Rev. Mol. Cell Biol. 6: 386-398.
81. Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genomics 283: 185-196.
82. McClung, C.R. (2006). Plant circadian rhythms. Plant Cell 18: 792-803.
83. McGlincy, N.J., and Smith, C.W. (2008). Alternative splicing resulting in nonsense-mediated mRNA decay: What is the meaning of nonsense? Trends Biochem. Sci. 33: 385-393.
84. McKibbin, R.S., Wilkinson, M.D., Bailey, P.C., Flintham, J.E., Andrew, L.M., Lazzeri, P.A., Gale, M.D., Lenton, J.R., and Holdsworth, M.J. (2002). Transcripts of Vp-1 homeologues are misspliced in modern wheat and ancestral species. Proc. Natl. Acad. Sci. USA 99: 10203-10208.
85. Moll, C., von Lyncker, L., Zimmermann, S., Kägi, C., Baumann, N., Twell, D., Grossniklaus, U., and Gross-Hardt, R. (2008). CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56: 913-921.
86. Monaghan, J., Xu, F., Gao, M., Zhao, Q., Palma, K., Long, C., Chen, S., Zhang, Y., and Li, X. (2009). Two Prp19-like U-box proteins in the MOS4-associated complex play redundant roles in plant innate immunity. PLoS Pathog. 5: e1000526.
87. Monaghan, J., Xu, F., Xu, S., Zhang, Y., and Li, X. (2010). Two putative RNA-binding proteins function with unequal genetic redundancy in the MOS4-associated complex. Plant Physiol. 154: 1783-1793.
88. Moreno, J.E., Shyu, C., Campos, M.L., Patel, L.C., Chung, H.S., Yao, J., He, S.Y., and Howe, G.A. (2013). Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiol. 162: 1006-1017.
89. Nakashima, K., Ito, Y., and Yamaguchi-Shinozaki, K. (2009). Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149: 88-95.
90. Nagashima, Y., Mishiba, K.-i., Suzuki, E., Shimada, Y., Iwata, Y., and Koizumi, N. (2011). Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci. Rep. 1: 29.
91. Nicaise, V., Joe, A., Jeong, B., Korneli, C., Boutrot, F., Wested, I., Staiger, D., Alfano, J.R., and Zipfel, C. (2013). Pseudomonas HopU1 affects interaction of plant immune receptor mRNAs to the RNA-binding protein GRP7. EMBO J. 32: 701-712.
92. Nicholson, P., and Mühlemann, O. (2010). Cutting the nonsense: The degradation of PTC-containing mRNAs. Biochem. Soc. Trans. 38: 1615-1620.
93. Nilsen, T.W., and Graveley, B.R. (2010). Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
94. Nlend Nlend, R., Meyer, K., and Schümperli, D. (2010). Repair of pre-mRNA splicing: Prospects for a therapy for spinal muscular atrophy. RNA Biol. 7: 430-440.
95. Ossowski, S., Schneeberger, K., Clark, R.M., Lanz, C., Warthmann, N., and Weigel, D. (2008). Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18: 2024-2033.
96. Palma, K., Zhao, Q., Cheng, Y.T., Bi, D., Monaghan, J., Cheng, W., Zhang, Y., and Li, X. (2007). Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev. 21: 1484-1493.
97. Palusa, S.G., Ali, G.S., and Reddy, A.S. (2007). Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J. 49: 1091-1107.
98. Papp, I., Mur, L.A., Dalmadi, A., Dulai, S., and Koncz, C. (2004). A mutation in the Cap Binding Protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol. Biol. 55: 679-686.
99. Perea-Resa, C., Hernández-Verdeja, T., López-Cobollo, R., del Mar Castellano, M., and Salinas, J. (2012). LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell 24: 4930-4947.
100. Posé, D., Verhage, L., Ott, F., Yant, L., Mathieu, J., Angenent, G.C., Immink, R.G.H., and Schmid, M. (September 25, 2013). Temperaturedependent regulation of flowering by antagonistic FLM variants. Nature (online), doi/10.1038/nature12633.
101. Raczynska, K.D., Simpson, C.G., Ciesiolka, A., Szewc, L., Lewandowska, D., McNicol, J., Szweykowska-Kulinska, Z., Brown, J.W., and Jarmolowski, A. (2010). Involvement of the nuclear cap-binding protein complex in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res. 38: 265-278.
102. Rasche, N., Dybkov, O., Schmitzová, J., Akyildiz, B., Fabrizio, P., and Lührmann, R. (2012). Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. EMBO J. 31: 1591-1604.
103. Rausin, G., Tillemans, V., Stankovic, N., Hanikenne, M., and Motte, P. (2010). Dynamic nucleocytoplasmic shuttling of an Arabidopsis SR splicing factor: role of the RNA-binding domains. Plant Physiol. 153: 273-284.
104. Rayson, S., Arciga-Reyes, L., Wootton, L., De Torres Zabala, M., Truman, W., Graham, N., Grant, M., and Davies, B. (February 22, 2012). A role for nonsense-mediated mRNA decay in plants: Pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLoS ONE 7: e31917.
105. Reddy, A.S.N., Marquez, Y., Kalyna, M., and Barta, A. (2013). Complexity of the alternative splicing landscape in plants. Plant Cell. 25: 3658-3684.
106. Remy, E., Cabrito, T.R., Baster, P., Batista, R.A., Teixeira, M.C., Friml, J., Sá-Correia, I., and Duque, P. (2013). A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 25: 901-926.
107. 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.
108. Rosloski, S.M., Singh, A., Jali, S.S., Balasubramanian, S., Weigel, D., and Grbic, V. (2013). Functional analysis of splice variant expression of MADS AFFECTING FLOWERING 2 of Arabidopsis thaliana. Plant Mol. Biol. 81: 57-69.
109. Rühl, C., Stauffer, E., Kahles, A., Wagner, G., Drechsel, G., Rätsch, G., and Wachter, A. (2012). Polypyrimidine tract binding protein homologs from Arabidopsis are key regulators of alternative splicing with implications in fundamental developmental processes. Plant Cell 24: 4360-4375.
110. Saltzman, A.L., Pan, Q., and Blencowe, B.J. (2011). Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev. 25: 373-384.
111. Sanchez, S.E., et al. (2010). A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468: 112-116.
112. Scaffidi, P., Gordon, L., and Misteli, T. (2005). The cell nucleus and aging: Tantalizing clues and hopeful promises. PLoS Biol. 3: e395.
113. Schmal, C., Reimann, P., and Staiger, D. (2013). A circadian clockregulated toggle switch explains AtGRP7 and AtGRP8 oscillations in Arabidopsis thaliana. PLoS Comput. Biol. 9: e1002986.
114. Schmidt, F., Marnef, A., Cheung, M.-K., Wilson, I., Hancock, J., Staiger, D., and Ladomery, M. (2010). A proteomic analysis of oligo(dT)-bound mRNP containing oxidative stress-induced Arabidopsis thaliana RNA-binding proteins ATGRP7 and ATGRP8. Mol. Biol. Rep. 37: 839-845.
115. Schöning, J.C., and Staiger, D. (2005). At the pulse of time: Protein interactions determine the pace of circadian clocks. FEBS Lett. 579: 3246-3252.
116. Schöning, 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.
117. Sen, R., and Fugmann, S.D. (2012). Transcription, splicing, and release: Are we there yet? Cell 150: 241-243.
118. Seo, P.J., Hong, S.-Y., Kim, S.-G., and Park, C.-M. (2011a). Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci. 16: 541-549.
119. Seo, P.J., Kim, M.J., Ryu, J.-Y., Jeong, E.-Y., and Park, C.-M. (2011a). Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nat. Commun. 2: 303.
120. Seo, P.J., Park, M.-J., Lim, M.-H., Kim, S.-G., Lee, M., Baldwin, I.T., and Park, C.-M. (2011b). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24: 2427-2442.
121. Severing, E.I., van Dijk, A.D.J., Morabito, G., Busscher-Lange, J., Immink, R.G.H., and van Ham, R.C.H.J. (January 25, 2012). Predicting the impact of alternative splicing on plant MADS domain protein function. PLoS ONE 7: e30524.
122. Shi, C., Baldwin, I.T., and Wu, J. (2012). Arabidopsis plants having defects in nonsense-mediated mRNA decay factors UPF1, UPF2, and UPF3 show photoperiod-dependent phenotypes in development and stress responses. J. Integr. Plant Biol. 54: 99-114.
123. Simpson, C.G., Fuller, J., Maronova, M., Kalyna, M., Davidson, D., McNicol, J., Barta, A., and Brown, J.W. (2008). Monitoring changes in alternative precursor messenger RNA splicing in multiple gene transcripts. Plant J. 53: 1035-1048.
124. Song, H.-R., Song, J.-D., Cho, J.-N., Amasino, R.M., Noh, B., and Noh, Y.-S. (2009). The RNA binding protein ELF9 directly reduces SUPPRESSOR OF OVEREXPRESSION OF CO1 transcript levels in arabidopsis, possibly via nonsense-mediated mRNA decay. Plant Cell 21: 1195-1211.
125. Spartz, A.K., Herman, R.K., and Shaw, J.E. (2004). SMU-2 and SMU-1, Caenorhabditis elegans homologs of mammalian spliceosomeassociated proteins RED and fSAP57, work together to affect splice site choice. Mol. Cell. Biol. 24: 6811-6823.
126. Staiger, D., Korneli, C., Lummer, M., and Navarro, L. (2013). Emerging role for RNA-based regulation in plant immunity. New Phytol. 197: 394-404.
127. Stamm, S., Ben-Ari, S., Rafalska, I., Tang, Y., Zhang, Z., Toiber, D., Thanaraj, T.A., and Soreq, H. (2005). Function of alternative splicing. Gene 344: 1-20.
128. Stauffer, E., Westermann, A., Wagner, G., and Wachter, A. (2010). Polypyrimidine tract-binding protein homologues from Arabidopsis underlie regulatory circuits based on alternative splicing and downstream control. Plant J. 64: 243-255.
129. Streitner, C., Hennig, L., Korneli, C., and Staiger, D. (2010). Global transcript profiling of transgenic plants constitutively overexpressing the RNA-binding protein AtGRP7. BMC Plant Biol. 10: 221.
130. Streitner, C., Köster, T., Simpson, C.G., Shaw, P., Danisman, S., Brown, J.W.S., and Staiger, D. (2012). An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana. Nucleic Acids Res. 40: 11240-11255.
131. Streitner, C., Simpson, C.G., Shaw, P., Danisman, S., Brown, J.W. S., and Staiger, D. (2013). Small changes in ambient temperature affect alternative splicing in Arabidopsis thaliana. Plant Signal. Behav. 8: e24638.
132. Sugio, A., Dreos, R., Aparicio, F., and Maule, A.J. (2009). The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 21: 642-654.
133. Sugliani, M., Brambilla, V., Clerkx, E.J., Koornneef, M., and Soppe, W.J. (2010). The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in Arabidopsis. Plant Cell 22: 1936-1946.
134. Swaraz, A.M., Park, Y.D., and Hur, Y. (2011). Knock-out mutations of Arabidopsis SmD3-b induce pleotropic phenotypes through altered transcript splicing. Plant Sci. 180: 661-671.
135. Syed, N.H., Kalyna, M., Marquez, Y., Barta, A., and Brown, J.W.S. (2012). Alternative splicing in plants-Coming of age. Trends Plant Sci. 17: 616-623.
136. Tanabe, N., Yoshimura, K., Kimura, A., Yabuta, Y., and Shigeoka, S. (2007). Differential expression of alternatively spliced mRNAs of Arabidopsis SR protein homologs, atSR30 and atSR45a, in response to environmental stress. Plant Cell Physiol. 48: 1036-1049.
137. Tazi, J., Bakkour, N., and Stamm, S. (2009). Alternative splicing and disease. Biochim. Biophys. Acta 1792: 14-26.
138. Tharun, S. (2009). Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell. Mol. Biol. 272: 149-189.
139. The Potato Genome Sequencing Consortium (2011). Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195.
140. Thomas, J., Palusa, S.G., Prasad, K.V.S.K., Ali, G.S., Surabhi, G.-K., Ben-Hur, A., Abdel-Ghany, S.E., and Reddy, A.S.N. (2012). Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA. Plant J. 72: 935-946.
141. Tillemans, V., Dispa, L., Remacle, C., Collinge, M., and Motte, P. (2005). Functional distribution and dynamics of Arabidopsis SR splicing factors in living plant cells. Plant J. 41: 567-582.
142. Tillemans, V., Leponce, I., Rausin, G., Dispa, L., and Motte, P. (2006). Insights into nuclear organization in plants as revealed by the dynamic distribution of Arabidopsis SR splicing factors. Plant Cell 18: 3218-3234.
143. Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J., and Katagiri, F. (2009). Network properties of robust immunity in plants. PLoS Genet. 5: e1000772.
144. Venables, J.P., et al. (2009). Cancer-associated regulation of alternative splicing. Nat. Struct. Mol. Biol. 16: 670-676.
145. Villarreal, N.M., Rosli, H.G., Marti{dotless}nez, G.A., and Civello, P.M. (2008). Polygalacturonase activity and expression of related genes during ripening of strawberry cultivars with contrasting fruit firmness. Postharvest Biol. Technol. 47: 141-150.
146. von Koskull-Döring, P., Scharf, K.D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12: 452-457.
147. Wachter, A., Rühl, C., and Stauffer, E. (2012). The role of polypyrimidine tract-binding proteins and other hnRNP proteins in plant splicing regulation. Front. Plant Sci. 3: 81.
148. Wahl, M.C., Will, C.L., and Lührmann, R. (2009). The spliceosome: Design principles of a dynamic RNP machine. Cell 136: 701-718.
149. Walters, B., Lum, G., Sablok, G., and Min, X.J. (2013). Genome-wide landscape of alternative splicing events in Brachypodium distachyon. DNA Res. 20: 163-171.
150. Wang, C., Tian, Q., Hou, Z., Mucha, M., Aukerman, M., and Olsen, O.A. (2007). The Arabidopsis thaliana AT PRP39-1 gene, encoding a tetratricopeptide repeat protein with similarity to the yeast premRNA processing protein PRP39, affects flowering time. Plant Cell Rep. 26: 1357-1366.
151. Wang, X., et al. (2012). SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24: 3278-3295.
152. Weber, A.P.M., Weber, K.L., Carr, K., Wilkerson, C., and Ohlrogge, J.B. (2007). Sampling the Arabidopsis transcriptome with massively parallel pyrosequencing. Plant Physiol. 144: 32-42.
153. Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C., and Baker, B. (1994). The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.
154. Will, C.L., and Lührmann, R. (2011). Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 3: a003707.
155. Windram, O., et al. (2012). Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24: 3530-3557.
156. Witten, J.T., and Ule, J. (2011). Understanding splicing regulation through RNA splicing maps. Trends Genet. 27: 89-97.
157. Xiong, L., Gong, Z., Rock, C.D., Subramanian, S., Guo, Y., Xu, W., Galbraith, D., and Zhu, J.K. (2001). Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev. Cell 1: 771-781.
158. Xu, F., Xu, S., Wiermer, M., Zhang, Y., and Li, X. (2012a). The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes. Plant J. 70: 916-928.
159. Xu, S., Zhang, Z., Jing, B., Gannon, P., Ding, J., Xu, F., Li, X., and Zhang, Y. (2012b). Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genet. 7: e1002159.
160. Yan, K., Liu, P., Wu, C.-A., Yang, G.-D., Xu, R., Guo, Q.-H., Huang, J.-G., and Zheng, C.-C. (2012). Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol. Cell 48: 521-531.
161. Yi, Y., and Jack, T. (1998). An intragenic suppressor of the Arabidopsis floral organ identity mutant apetala3-1 functions by suppressing defects in splicing. Plant Cell 10: 1465-1477.
162. Yuan, Y., Chung, J.-D., Fu, X., Johnson, V.E., Ranjan, P., Booth, S.L., Harding, S.A., and Tsai, C.-J. (2009). Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 22020-22025.
163. Zhang, C.-J., Zhou, J.-X., Liu, J., Ma, Z.-Y., Zhang, S.-W., Dou, K., Huang, H.-W., Cai, T., Liu, R., Zhu, J.-K., and He, X.-J. (2013). The splicing machinery promotes RNA-directed DNA methylation and transcriptional silencing in Arabidopsis. EMBO J. 32: 1128-1140.
164. Zhang, G., et al. (2010). Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res. 20: 646-654.
165. Zhang, N., Kallis, R.P., Ewy, R.G., and Portis, A.R., Jr.,. (2002). Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc. Natl. Acad. Sci. USA 99: 3330-3334.
166. Zhang, X.C., and Gassmann, W. (2003). RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 15: 2333-2342.
167. Zhang, X.-C., and Gassmann, W. (2007). Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol. 145: 1577-1587.
168. Zhang, X.N., and Mount, S.M. (2009). Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development. Plant Physiol. 150: 1450-1458.
169. Zhang, Y., Goritschnig, S., Dong, X., and Li, X. (2003). A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636-2646.
170. Zhang, Z., et al. (2011). Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23: 396-411.