603
Views
16
CrossRef citations to date
0
Altmetric
Articles

Emerging Functions of Plant Serine/Arginine-Rich (SR) Proteins: Lessons from Animals

, , , &

References

  • Ajiro, M., Jia, R., Yang, Y., Zhu, J., and Zheng, Z. M. 2016. A genome landscape of SRSF3-regulated splicing events and gene expression in human osteosarcoma U2OS cells. Nucleic Acids Res. 44: 1854–1870.
  • Albaqami, M., Laluk, K., and Reddy, A. S. 2019. The Arabidopsis splicing regulator SR45 confers salt tolerance in a splice isoform-dependent manner. Plant Mol. Biol. 100: 379–390.
  • Albaqami, M. and Reddy, A. S. 2018. Development of an in vitro pre-mRNA splicing assay using plant nuclear extract. Plant Meth. 14: 1.
  • 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.
  • Ali, G. S., Palusa, S. G., Golovkin, M., Prasad, J., Manley, J. L., and Reddy, A. S. 2007. Regulation of plant developmental processes by a novel splicing factor. PLOS One. 2: e471.
  • Ali, G. S. and Reddy, A. S. 2006. ATP, phosphorylation and transcription regulate the mobility of plant splicing factors. J. Cell Sci. 119: 3527–3538.
  • Anczuków, O., Akerman, M., Cléry, A., Wu, J., Shen, C., Shirole, N. H., Raimer, A., Sun, S., Jensen, M. A., Hua, Y., Allain, F. H.-T., and Krainer, A. R. 2015. SRSF1-regulated alternative splicing in breast cancer. Mol. Cell. 60: 105–117.
  • Anczuków, O., Rosenberg, A. Z., Akerman, M., Das, S., Zhan, L., Karni, R., Muthuswamy, S. K., and Krainer, A. R. 2012. The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation. Nat. Struct. Mol. Biol. 19: 220–228.
  • Anko, M. L. 2014. Regulation of gene expression programmes by serine-arginine rich splicing factors. Semin. Cell Dev. Biol. 32: 11–21.
  • Anko, M. L., Muller-McNicoll, M., Brandl, H., Curk, T., Gorup, C., Henry, I., Ule, J., and Neugebauer, K. M. 2012. The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol. 13: R17.
  • Ast, G. 2004. How did alternative splicing evolve? Nat. Rev. Genet. 5: 773–782.
  • Aubol, B. E., Wu, G., Keshwani, M. M., Movassat, M., Fattet, L., Hertel, K. J., Fu, X. D., and Adams, J. A. 2016. Release of SR proteins from CLK1 by SRPK1: a symbiotic kinase system for phosphorylation control of pre-mRNA splicing. Mol. Cell. 63: 218–228.
  • Aznarez, I., Nomakuchi, T. T., Tetenbaum-Novatt, J., Rahman, M. A., Fregoso, O., Rees, H., and Krainer, A. R. 2018. Mechanism of nonsense-mediated mRNA decay stimulation by splicing factor SRSF1. Cell Rep. 23: 2186–2198.
  • Barbosa-Morais, N. L., Carmo-Fonseca, M., and Aparício, S. 2006. Systematic genome-wide annotation of spliceosomal proteins reveals differential gene family expansion. Genome Res. 16: 66–77.
  • Barta, A., Kalyna, M., and Reddy, A. S. 2010. Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell. 22: 2926–2929.
  • Barta, A., Marquez, Y., and Brown, J. W. 2012. Challenges in plant alternative splicing. In Alternative Pre‐mRNA Splicing: Theory and Protocols; Stamm, S., Smith, C., and Lührmann, R., Eds. Wiley: New York, NY, pp 79–91.
  • Bedard, K. M., Daijogo, S., and Semler, B. L. 2007. A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J. 26: 459–467.
  • Birney, E., Kumar, S., and Krainer, A. R. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21: 5803–5816.
  • Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72: 291–336.
  • Blencowe, B. J. 2017. The relationship between alternative splicing and proteomic complexity. Trends Biochem. Sci. 42: 407–408.
  • Botti, V., McNicoll, F., Steiner, M. C., Richter, F. M., Solovyeva, A., Wegener, M., Schwich, O. D., Poser, I., Zarnack, K., Wittig, I., Neugebauer, K. M., and Muller-McNicoll, M. 2017. Cellular differentiation state modulates the mRNA export activity of SR proteins. J. Cell Biol. 216: 1993–2009.
  • Bourgeois, C. F., Lejeune, F., and Stevenin, J. 2004. Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA. Prog. Nucleic Acid Res. Mol. Biol. 78: 37–88.
  • Brugiolo, M., Botti, V., Liu, N., Muller-McNicoll, M., and Neugebauer, K. M. 2017. Fractionation iCLIP detects persistent SR protein binding to conserved, retained introns in chromatin, nucleoplasm and cytoplasm. Nucleic Acids Res. 45: 10452–10465.
  • Busch, A. and Hertel, K. J. 2012. Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip Rev RNA 3: 1–12.
  • Butt, H., Piatek, A., Li, L., Reddy, A. S., and Mahfouz, M. M. 2019. Multiplex CRISPR mutagenesis of the serine/arginine-rich (SR) gene family in rice. Genes 10: 596.
  • Cáceres, J. F. and Kornblihtt, A. R. 2002. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18: 186–193.
  • Caceres, J. F. and Krainer, A. R. 1993. Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J. 12: 4715–4726.
  • Caceres, J. F., Misteli, T., Screaton, G. R., Spector, D. L., and Krainer, A. R. 1997. Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138: 225–238.
  • Caceres, J. F., Screaton, G. R., and Krainer, A. R. 1998. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12: 55–66.
  • Califice, S., Baurain, D., Hanikenne, M., and Motte, P. 2012. A single ancient origin for prototypical serine/arginine-rich splicing factors. Plant Physiol. 158: 546–560.
  • Cao, W., Jamison, S. F., and Garcia-Blanco, M. A. 1997. Both phosphorylation and dephosphorylation of ASF/SF2 are required for pre-mRNA splicing in vitro. RNA 3: 1456–1467.
  • Carvalho, R. F., Carvalho, S. D., and Duque, P. 2010. The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol. 154: 772–783.
  • Carvalho, R. F., Feijao, C. V., and Duque, P. 2013. On the physiological significance of alternative splicing events in higher plants. Protoplasma 250: 639–650.
  • Carvalho, R. F., Szakonyi, D., Simpson, C. G., Barbosa, I. C., Brown, J. W., Baena-González, E., and Duque, P. 2016. The Arabidopsis SR45 splicing factor, a negative regulator of sugar signaling, modulates SNF1-related protein kinase 1 stability. Plant Cell. 28: 1910–1925.
  • Cavaloc, Y., Bourgeois, C. F., Kister, L., and Stevenin, J. 1999. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA 5: 468–483.
  • Cavaloc, Y., Popielarz, M., Fuchs, J. P., Gattoni, R., and Stevenin, J. 1994. Characterization and cloning of the human splicing factor 9G8: a novel 35 kDa factor of the serine/arginine protein family. EMBO J. 13: 2639–2649.
  • Cazalla, D., Zhu, J., Manche, L., Huber, E., Krainer, A. R., and Caceres, J. F. 2002. Nuclear export and retention signals in the RS domain of SR proteins. Mol. Cell. Biol. 22: 6871–6882.
  • Chen, M. X., Zhu, F. Y., Gao, B., Ma, K.-L., Zhang, Y., Fernie, A. R., Chen, X., Dai, L., Ye, N. H., Zhang, X., Tian, Y., Zhang, D., Xiao, S., Zhang, J., and Liu, Y. G. 2020. Full-length transcript-based proteogenomics of rice improves its genome and proteome annotation. Plant Physiol. 182: 1510–1526.
  • Chen, S., Li, J., Liu, Y., and Li, H. 2019. Genome-wide analysis of serine/arginine-rich protein family in wheat and Brachypodium distachyon. Plants 8: 188.
  • Chen, T., Cui, P., Chen, H., Ali, S., Zhang, S., and Xiong, L. 2013. A KH-domain RNA-binding protein interacts with FIERY2/CTD phosphatase-like 1 and splicing factors and is important for pre-mRNA splicing in Arabidopsis. PLOS Genet. 9: e1003875.
  • Chen, T., Cui, P., and Xiong, L. 2015. The RNA-binding protein HOS5 and serine/arginine-rich proteins RS40 and RS41 participate in miRNA biogenesis in Arabidopsis. Nucleic Acids Res. 43: 8283–8298.
  • Cho, S., Hoang, A., Sinha, R., Zhong, X. Y., Fu, X. D., Krainer, A. R., and Ghosh, G. 2011. Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly. Proc. Natl. Acad. Sci. USA. 108: 8233–8238.
  • Cléry, A., Sinha, R., Anczuków, O., Corrionero, A., Moursy, A., Daubner, G. M., Valcárcel, J., Krainer, A. R., and Allain, F. H. T. 2013. Isolated pseudo-RNA-recognition motifs of SR proteins can regulate splicing using a noncanonical mode of RNA recognition. Proc. Natl. Acad. Sci. USA. 110: E2802–E2811.
  • Cohen-Eliav, M., Golan-Gerstl, R., Siegfried, Z., Andersen, C. L., Thorsen, K., Ørntoft, T. F., Mu, D., and Karni, R. 2013. The splicing factor SRSF6 is amplified and is an oncoprotein in lung and colon cancers. J. Pathol. 229: 630–639.
  • Colwill, K., Pawson, T., Andrews, B., Prasad, J., Manley, J. L., Bell, J. C., and Duncan, P. I. 1996. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15: 265–275.
  • Das, R., Dufu, K., Romney, B., Feldt, M., Elenko, M., and Reed, R. 2006. Functional coupling of RNAP II transcription to spliceosome assembly. Genes Dev. 20: 1100–1109.
  • Das, S., Anczuków, O., Akerman, M., and Krainer, A. R. 2012. Oncogenic splicing factor SRSF1 is a critical transcriptional target of MYC. Cell Rep. 1: 110–117.
  • Day, I. S., Golovkin, M., Palusa, S. G., Link, A., Ali, G. S., Thomas, J., Richardson, D. N., and Reddy, A. S. 2012. Interactions of SR45, an SR-like protein, with spliceosomal proteins and an intronic sequence: insights into regulated splicing. Plant J. 71: 936–947.
  • de Francisco Amorim, M., Willing, E. M., Szabo, E. X., Francisco-Mangilet, A. G., Droste-Borel, I., Maček, B., Schneeberger, K., and Laubinger, S. 2018. The U1 snRNP subunit LUC7 modulates plant development and stress responses via regulation of alternative splicing. Plant Cell. 30: 2838–2854.
  • de la Fuente van Bentem, S., Anrather, D., Roitinger, E., Djamei, A., Hufnagl, T., Barta, A., Csaszar, E., Dohnal, I., Lecourieux, D., and Hirt, H. 2006. Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Res. 34: 3267–3278.
  • Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475–1489.
  • Ding, F., Cui, P., Wang, Z., Zhang, S., Ali, S., and Xiong, L. 2014. Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genomics. 15: 431.
  • Ding, J. H., Xu, X., Yang, D., Chu, P. H., Dalton, N. D., Ye, Z., Yeakley, J. M., Cheng, H., Xiao, R. P., Ross, J., Chen, J., and Fu, X. D. 2004. Dilated cardiomyopathy caused by tissue-specific ablation of SC35 in the heart. EMBO J. 23: 885–896.
  • Docquier, S., Tillemans, V., Deltour, R., and Motte, P. 2004. Nuclear bodies and compartmentalization of pre-mRNA splicing factors in higher plants. Chromosoma 112: 255–266.
  • Drechsel, G., Kahles, A., Kesarwani, A. K., Stauffer, E., Behr, J., Drewe, P., Ratsch, G., and Wachter, A. 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.
  • Drexler, H. L., Choquet, K., and Churchman, L. S. 2020. Splicing kinetics and coordination revealed by direct nascent RNA sequencing through nanopores. Mol. Cell. 77: 985–998.
  • Duque, P. 2011. A role for SR proteins in plant stress responses. Plant Signal Behav. 6: 49–54.
  • Fang, Y., Hearn, S., and Spector, D. L. 2004. Tissue-specific expression and dynamic organization of SR splicing factors in Arabidopsis. Mol. Biol. Cell. 15: 2664–2673.
  • Fededa, J. P. and Kornblihtt, A. R. 2008. A splicing regulator promotes transcriptional elongation. Nat. Struct. Mol. Biol. 15: 779–781.
  • Feilner, T., Hultschig, C., Lee, J., Meyer, S., Immink, R. G., Koenig, A., Possling, A., Seitz, H., Beveridge, A., Scheel, D., Cahill, D. J., Lehrach, H., Kreutzberger, J., and Kersten, B. 2005. High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol. Cell Proteom. 4: 1558–1568.
  • Filichkin, S., Priest, H. D., Megraw, M., and Mockler, T. C. 2015. Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress. Curr. Opin. Plant Biol. 24: 125–135.
  • Fischer, D. C., Noack, K., Runnebaum, I. B., Watermann, D. O., Kieback, D. G., Stamm, S., and Stickeler, E. 2004. Expression of splicing factors in human ovarian cancer. Oncol. Rep. 11: 1085–1090.
  • Forment, J., Naranjo, M. Á., Roldán, M., Serrano, R., and Vicente, O. 2002. Expression of Arabidopsis SR-like splicing proteins confers salt tolerance to yeast and transgenic plants. Plant J. 30: 511–519.
  • Fu, X. D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1: 663–680.
  • Fu, X. D. and Maniatis, T. 1990. Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343: 437–441.
  • Fu, X. D., Mayeda, A., Maniatis, T., and Krainer, A. R. 1992. General splicing factors SF2 and SC35 have equivalent activities in vitro, and both affect alternative 5′ and 3′ splice site selection. Proc. Natl. Acad. Sci. USA. 89: 11224–11228.
  • Galganski, L., Urbanek, M. O., and Krzyzosiak, W. J. 2017. Nuclear speckles: molecular organization, biological function and role in disease. Nucleic Acids Res. 45: 10350–10368.
  • Ge, H. and Manley, J. L. 1990. A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell 62: 25–34.
  • Ghigna, C., Giordano, S., Shen, H., Benvenuto, F., Castiglioni, F., Comoglio, P. M., Green, M. R., Riva, S., and Biamonti, G. 2005. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell. 20: 881–890.
  • Göhring, J., Jacak, J., and Barta, A. 2014. Imaging of endogenous messenger RNA splice variants in living cells reveals nuclear retention of transcripts inaccessible to nonsense-mediated decay in Arabidopsis. Plant Cell. 26: 754–764.
  • Golovkin, M. and Reddy, A. S. 1998. The plant U1 small nuclear ribonucleoprotein particle 70K protein interacts with two novel serine/arginine-rich proteins. Plant Cell. 10: 1637–1648.
  • Golovkin, M. and Reddy, A. S. 1999. An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein. J. Biol. Chem. 274: 36428–36438.
  • Gonçalves, V., Henriques, A. F. A., Henriques, A., Pereira, J. F. S., Pereira, J., Neves Costa, A., Moyer, M. P., Moita, L. F., Gama-Carvalho, M., Matos, P., and Jordan, P. 2014. Phosphorylation of SRSF1 by SRPK1 regulates alternative splicing of tumor-related Rac1b in colorectal cells. RNA 20: 474–482.
  • Graveley, B. R. 2000. Sorting out the complexity of SR protein functions. RNA 6: 1197–1211.
  • Graveley, B. R., Hertel, K. J., and Maniatis, T. 2001. The role of U2AF35 and U2AF65 in enhancer-dependent splicing. RNA 7: 806–818.
  • Gu, J., Ma, S., Zhang, Y., Wang, D., Cao, S., and Wang, Z. Y. 2020. Genome-wide identification of cassava serine/arginine-rich proteins: insights into alternative splicing of pre-mRNAs and response to abiotic stress. Plant Cell Physiol. 61: 178–191.
  • Gu, J., Xia, Z., Luo, Y., Jiang, X., Qian, B., Xie, H., Zhu, J. K., Xiong, L., Zhu, J., and Wang, Z. Y. 2018. Spliceosomal protein U1A is involved in alternative splicing and salt stress tolerance in Arabidopsis thaliana. Nucleic Acids Res. 46: 1777–1792.
  • Gui, J. F., Lane, W. S., and Fu, X. D. 1994. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369: 678–682.
  • Han, J., Xiong, J., Wang, D., and Fu, X. D. 2011. Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol. 21: 336–343.
  • Hanamura, A., Cáceres, J. F., Mayeda, A., Franza, B. R., and Krainer, A. R. 1998. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4: 430–444.
  • Hartmann, L., Wießner, T., and Wachter, A. 2018. Subcellular compartmentation of alternatively spliced transcripts defines SERINE/ARGININE-RICH PROTEIN30 expression. Plant Physiol. 176: 2886–2903.
  • Hertel, K. J. and Graveley, B. R. 2005. RS domains contact the pre-mRNA throughout spliceosome assembly. Trends Biochem. Sci. 30: 115–118.
  • Hertel, K. J. and Maniatis, T. 1999. Serine-arginine (SR)-rich splicing factors have an exon-independent function in pre-mRNA splicing. Proc. Natl. Acad. Sci. USA. 96: 2651–2655.
  • Herzel, L., Straube, K., and Neugebauer, K. M. 2018. Long-read sequencing of nascent RNA reveals coupling among RNA processing events. Genome Res. 28: 1008–1019.
  • Heyer, E. E. and Moore, M. J. 2016. Redefining the translational status of 80S monosomes. Cell 164: 757–769.
  • Howard, J. M. and Sanford, J. R. 2015. The RNAissance family: SR proteins as multifaceted regulators of gene expression. Wiley Interdiscip. Rev. RNA. 6: 93–110.
  • Huang, Y., Gattoni, R., Stevenin, J., and Steitz, J. A. 2003. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell. 11: 837–843.
  • Huang, Y., Yario, T. A., and Steitz, J. A. 2004. A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl. Acad. Sci. USA. 101: 9666–9670.
  • Iida, K. and Go, M. 2006. Survey of conserved alternative splicing events of mRNAs encoding SR proteins in land plants. Mol. Biol. Evol. 23: 1085–1094.
  • Isshiki, M., Tsumoto, A., and Shimamoto, K. 2006. The serine/arginine-rich protein family in rice plays important roles in constitutive and alternative splicing of pre-mRNA. Plant Cell. 18: 146–158.
  • Jakubauskiene, E., Vilys, L., Makino, Y., Poellinger, L., and Kanopka, A. 2015. Increased serine-arginine (SR) protein phosphorylation changes pre-mRNA splicing in hypoxia. J. Biol. Chem. 290: 18079–18089.
  • Jeong, S. 2017. SR proteins: binders, regulators, and connectors of RNA. Mol. Cells. 40: 1–9.
  • Ji, X., Zhou, Y., Pandit, S., Huang, J., Li, H., Lin, C. Y., Xiao, R., Burge, C. B., and Fu, X. D. 2013. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 153: 855–868.
  • Jiang, J., Liu, X., Liu, C., Liu, G., Li, S., and Wang, L. 2017. Integrating omics and alternative splicing reveals insights into grape response to high temperature. Plant Physiol. 173: 1502–1518.
  • Jiménez, M., Urtasun, R., Elizalde, M., Azkona, M., Latasa, M. U., Uriarte, I., Arechederra, M., Alignani, D., Bárcena-Varela, M., Álvarez-Sola, G., Colyn, L., Santamaría, E., Sangro, B., Rodriguez-Ortigosa, C., Fernández-Barrena, M. G., Ávila, M. A., and Berasain, C. 2019. Splicing events in the control of genome integrity: role of SLU7 and truncated SRSF3 proteins. Nucleic Acids Res. 47: 3450–3466.
  • Jumaa, H., Guenet, J., and Nielsen, P. 1997. Regulated expression and RNA processing of transcripts from the Srp20 splicing factor gene during the cell cycle. Mol. Cell. Biol. 17: 3116–3124.
  • Jumaa, H. and Nielsen, P. J. 1997. The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16: 5077–5085.
  • Jumaa, H. and Nielsen, P. J. 2000. Regulation of SRp20 exon 4 splicing. Biochim. Biophys. Acta. 1494: 137–143.
  • Jumaa, H., Wei, G., and Nielsen, P. J. 1999. Blastocyst formation is blocked in mouse embryos lacking the splicing factor SRp20. Curr. Biol. 9:899–902.
  • Kalyna, M. and Barta, A. 2004. A plethora of plant serine/arginine-rich proteins: redundancy or evolution of novel gene functions? Biochem. Soc. Trans. 32: 561–564.
  • 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.
  • 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.
  • Kalyna, M., Simpson, C. G., Syed, N. H., Lewandowska, D., Marquez, Y., Kusenda, B., Marshall, J., Fuller, J., Cardle, L., McNicol, J., Dinh, H. Q., Barta, A., and Brown, J. W. 2012. Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Res. 40: 2454–2469.
  • Kano, S., Nishida, K., Kurebe, H., Nishiyama, C., Kita, K., Akaike, Y., Kajita, K., Kurokawa, K., Masuda, K., Kuwano, Y., Tanahashi, T., and Rokutan, K. 2014. Oxidative stress-inducible truncated serine/arginine-rich splicing factor 3 regulates interleukin-8 production in human colon cancer cells. Am. J. Physiol. Cell Physiol. 306: C250–C262.
  • Karni, R., de Stanchina, E., Lowe, S. W., Sinha, R., Mu, D., and Krainer, A. R. 2007. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol. 14: 185–193.
  • Kataoka, N., Bachorik, J. L., and Dreyfuss, G. 1999. Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 145: 1145–1152.
  • Keren, H., Lev-Maor, G., and Ast, G. 2010. Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 11: 345–355.
  • Kohler, A. and Hurt, E. 2007. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8: 761–773.
  • Kohtz, J. D., Jamison, S. F., Will, C. L., Zuo, P., Luhrmann, R., Garcia-Blanco, M. A., and Manley, J. L. 1994. Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368: 119–124.
  • Koizumi, J., Okamoto, Y., Onogi, H., Mayeda, A., Krainer, A. R., and Hagiwara, M. 1999. The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs). J. Biol. Chem. 274: 11125–11131.
  • Köster, T. and Staiger, D. 2014. RNA-binding protein immunoprecipitation from whole-cell extracts. Meth. Mol. Biol. 1062: 679–695.
  • Krainer, A. R., Conway, G. C., and Kozak, D. 1990a. Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev. 4: 1158–1171.
  • Krainer, A. R., Conway, G. C., and Kozak, D. 1990b. The essential pre-mRNA splicing factor SF2 influences 5′ splice site selection by activating proximal sites. Cell 62: 35–42.
  • Krainer, A. R. and Maniatis, T. 1985. Multiple factors including the small nuclear ribonucleoproteins U1 and U2 are necessary for pre-mRNA splicing in vitro. Cell 42: 725–736.
  • Lai, M. C., Lin, R. I., and Tarn, W. Y. 2001. Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc. Natl. Acad. Sci. USA. 98: 10154–10159.
  • Lai, M. C. and Tarn, W. Y. 2004. Hypophosphorylated ASF/SF2 binds TAP and is present in messenger ribonucleoproteins. J. Biol. Chem. 279: 31745–31749.
  • Laloum, T., Martin, G., and Duque, P. 2018. Alternative splicing control of abiotic stress responses. Trends Plant Sci. 23: 140–150.
  • Lamond, A. I. and Spector, D. L. 2003. Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4: 605–612.
  • Lareau, L. F. and Brenner, S. E. 2015. Regulation of splicing factors by alternative splicing and NMD is conserved between kingdoms yet evolutionarily flexible. Mol. Biol. Evol. 32: 1072–1079.
  • Lareau, L. F., Inada, M., Green, R. E., Wengrod, J. C., and Brenner, S. E. 2007. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446: 926–929.
  • Lavigueur, A., La Branche, H., Kornblihtt, A. R., and Chabot, B. 1993. A splicing enhancer in the human fibronectin alternate ED1 exon interacts with SR proteins and stimulates U2 snRNP binding. Genes Dev. 7: 2405–2417.
  • Lazar, G., Schaal, T., Maniatis, T., and Goodman, H. M. 1995. Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc. Natl. Acad. Sci. USA. 92: 7672–7676.
  • Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J. L., and Lafyatis, R. 2002. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev. 16: 594–607.
  • Lewis, B. P., Green, R. E., and Brenner, S. E. 2003. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA. 100: 189–192.
  • Li, X. and Manley, J. L. 2005. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122: 365–378.
  • Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S., and Fu, X. D. 2008. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15: 819–826.
  • Lin, S., Xiao, R., Sun, P., Xu, X., and Fu, X. D. 2005. Dephosphorylation-dependent sorting of SR splicing factors during mRNP maturation. Mol. Cell. 20: 413–425.
  • Liu, H. X., Zhang, M., and Krainer, A. R. 1998. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev. 12: 1998–2012.
  • Liu, Y., Gonzalez-Porta, M., Santos, S., Brazma, A., Marioni, J. C., Aebersold, R., Venkitaraman, A. R., and Wickramasinghe, V. O. 2017. Impact of alternative splicing on the human proteome. Cell Rep. 20: 1229–1241.
  • Lopato, S., Forstner, C., Kalyna, M., Hilscher, J., Langhammer, U., Indrapichate, K., Lorkovic, Z. J., and 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: 39989–39998.
  • Lopato, S., Gattoni, R., Fabini, G., Stevenin, J., and Barta, A. 1999a. A novel family of plant splicing factors with a Zn knuckle motif: examination of RNA binding and splicing activities. Plant Mol. Biol. 39: 761–773.
  • Lopato, S., Kalyna, M., Dorner, S., Kobayashi, R., Krainer, A. R., and Barta, A. 1999b. atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev. 13: 987–1001.
  • Lopato, S., Mayeda, A., Krainer, A. R., and Barta, A. 1996a. Pre-mRNA splicing in plants: characterization of Ser/Arg splicing factors. Proc. Natl. Acad. Sci. USA. 93: 3074–3079.
  • Lopato, S., Waigmann, E., and Barta, A. 1996b. Characterization of a novel arginine/serine-rich splicing factor in Arabidopsis. Plant Cell. 8: 2255–2264.
  • Lorkovic, Z. J. and Barta, A. 2002. Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30: 623–635.
  • Lorkovic, Z. J., Hilscher, J., and Barta, A. 2004. Use of fluorescent protein tags to study nuclear organization of the spliceosomal machinery in transiently transformed living plant cells. Mol. Biol. Cell. 15: 3233–3243.
  • Lorkovic, Z. J., Hilscher, J., and Barta, A. 2008. Co-localisation studies of Arabidopsis SR splicing factors reveal different types of speckles in plant cell nuclei. Exp. Cell Res. 314: 3175–3186.
  • Maertens, G. N., Cook, N. J., Wang, W., Hare, S., Gupta, S. S., Oztop, I., Lee, K., Pye, V. E., Cosnefroy, O., Snijders, A. P., KewalRamani, V. N., Fassati, A., Engelman, A., and Cherepanov, P. 2014. Structural basis for nuclear import of splicing factors by human Transportin 3. Proc. Natl. Acad. Sci. USA. 111: 2728–2733.
  • Mahiet, C. and Swanson, C. M. 2016. Control of HIV-1 gene expression by SR proteins. Biochem. Soc. Trans. 44: 1417–1425.
  • Manley, J. L. and Krainer, A. R. 2010. A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes Dev. 24: 1073–1074.
  • Manley, J. L. and Tacke, R. 1996. SR proteins and splicing control. Genes Dev. 10: 1569–1579.
  • Maquat, L. E. 2004. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell Biol. 5: 89–99.
  • Marquez, Y., Brown, J. W. S., Simpson, C., Barta, A., and Kalyna, M. 2012. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res. 22: 1184–1195.
  • Maslon, M. M., Heras, S. R., Bellora, N., Eyras, E., and Caceres, J. F. 2014. The translational landscape of the splicing factor SRSF1 and its role in mitosis. Elife 3: e02028.
  • Mayeda, A., Screaton, G. R., Chandler, S. D., Fu, X. D., and Krainer, A. R. 1999. Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol. 19: 1853–1863.
  • 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.
  • Mermoud, J. E., Cohen, P. T., and Lamond, A. I. 1994. Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J. 13: 5679–5688.
  • Meseguer, S., Mudduluru, G., Escamilla, J. M., Allgayer, H., and Barettino, D. 2011. MicroRNAs-10a and -10b contribute to retinoic acid-induced differentiation of neuroblastoma cells and target the alternative splicing regulatory factor SFRS1 (SF2/ASF). J. Biol. Chem. 286: 4150–4164.
  • Michlewski, G., Sanford, J. R., and Caceres, J. F. 2008. The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol. Cell. 30: 179–189.
  • Misteli, T., Caceres, J. F., and Spector, D. L. 1997. The dynamics of a pre-mRNA splicing factor in living cells. Nature 387: 523–527.
  • Mori, T., Yoshimura, K., Nosaka, R., Sakuyama, H., Koike, Y., Tanabe, N., Maruta, T., Tamoi, M., and Shigeoka, S. 2012. Subcellular and subnuclear distribution of high-light responsive serine/arginine-rich proteins, atSR45a and atSR30, in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 76: 2075–2081.
  • Muller-McNicoll, M., Botti, V., de Jesus Domingues, A. M., Brandl, H., Schwich, O. D., Steiner, M. C., Curk, T., Poser, I., Zarnack, K., and Neugebauer, K. M. 2016. SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA export. Genes Dev. 30: 553–566.
  • Ngo, J. C., Chakrabarti, S., Ding, J. H., Velazquez-Dones, A., Nolen, B., Aubol, B. E., Adams, J. A., Fu, X. D., and Ghosh, G. 2005. Interplay between SRPK and Clk/Sty kinases in phosphorylation of the splicing factor ASF/SF2 is regulated by a docking motif in ASF/SF2. Mol. Cell. 20: 77–89.
  • Ni, J. Z., Grate, L., Donohue, J. P., Preston, C., Nobida, N., O’Brien, G., Shiue, L., Clark, T. A., Blume, J. E., and Ares, M. 2007. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 21: 708–718.
  • Nilsen, T. W. and Graveley, B. R. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457–463.
  • Nowak, D. G., Amin, E. M., Rennel, E. S., Hoareau-Aveilla, C., Gammons, M., Damodoran, G., Hagiwara, M., Harper, S. J., Woolard, J., Ladomery, M. R., and Bates, D. O. 2010. Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: a novel therapeutic strategy for angiogenesis. J. Biol. Chem. 285: 5532–5540.
  • 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.
  • Palusa, S. G. and Reddy, A. S. 2010. Extensive coupling of alternative splicing of pre-mRNAs of serine/arginine (SR) genes with nonsense-mediated decay. New Phytol. 185: 83–89.
  • Palusa, S. G. and Reddy, A. S. 2015. Differential recruitment of splice variants from SR pre-mRNAs to polysomes during development and in response to stresses. Plant Cell Physiol. 56: 421–427.
  • Pan, Q., Shai, O., Lee, L. J., Frey, B. J., and Blencowe, B. J. 2009. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 41: 762–762.
  • Pandit, S., Zhou, Y., Shiue, L., Coutinho-Mansfield, G., Li, H., Qiu, J., Huang, J., Yeo, G. W., Ares, M., and Fu, X. D. 2013. Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing. Mol. Cell. 50: 223–235.
  • Plass, M., Agirre, E., Reyes, D., Camara, F., and Eyras, E. 2008. Co-evolution of the branch site and SR proteins in eukaryotes. Trends Genet. 24: 590–594.
  • Popielarz, M., Cavaloc, Y., Mattei, M. G., Gattoni, R., and Stévenin, J. 1995. The gene encoding human splicing factor 9G8. Structure, chromosomal localization, and expression of alternatively processed transcripts. J. Biol. Chem. 270: 17830–17835.
  • Ramchatesingh, J., Zahler, A. M., Neugebauer, K. M., Roth, M. B., and Cooper, T. A. 1995. A subset of SR proteins activates splicing of the cardiac troponin T alternative exon by direct interactions with an exonic enhancer. Mol. Cell. Biol. 15: 4898–4907.
  • Rauch, H. B., Patrick, T. L., Klusman, K. M., Battistuzzi, F. U., Mei, W., Brendel, V. P., and Lal, S. K. 2014. Discovery and expression analysis of alternative splicing events conserved among plant SR proteins. Mol. Biol. Evol. 31: 605–613.
  • 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.
  • Reddy, A. S. and Shad Ali, G. 2011. Plant serine/arginine‐rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip. Rev. RNA. 2: 875–889.
  • Richardson, D. N., Rogers, M. F., Labadorf, A., Ben-Hur, A., Guo, H., Paterson, A. H., and Reddy, A. S. 2011. Comparative analysis of serine/arginine-rich proteins across 27 eukaryotes: insights into sub-family classification and extent of alternative splicing. PLoS One. 6: e24542.
  • Ring, H. Z. and Lis, J. T. 1994. The SR protein B52/SRp55 is essential for Drosophila development. Mol. Cell. Biol. 14: 7499–7506.
  • Risso, G., Pelisch, F., Quaglino, A., Pozzi, B., and Srebrow, A. 2012. Regulating the regulators: serine/arginine-rich proteins under scrutiny. IUBMB Life 64: 809–816.
  • Roscigno, R. F. and Garcia-Blanco, M. A. 1995. SR proteins escort the U4/U6.U5 tri-snRNP to the spliceosome. RNA 1: 692–706.
  • Roth, M. B., Zahler, A. M., and Stolk, J. A. 1991. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J. Cell Biol. 115: 587–596.
  • Sanford, J. R., Coutinho, P., Hackett, J. A., Wang, X., Ranahan, W., and Caceres, J. F. 2008. Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLOS One. 3: e3369.
  • Sanford, J. R., Ellis, J. D., Cazalla, D., and Caceres, J. F. 2005. Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl. Acad. Sci. USA. 102: 15042–15047.
  • Sanford, J. R., Gray, N. K., Beckmann, K., and Caceres, J. F. 2004. A novel role for shuttling SR proteins in mRNA translation. Genes Dev. 18: 755–768.
  • Sanford, J. R., Wang, X., Mort, M., Vanduyn, N., Cooper, D. N., Mooney, S. D., Edenberg, H. J., and Liu, Y. 2009. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 19: 381–394.
  • Sapra, A. K., Anko, M. L., Grishina, I., Lorenz, M., Pabis, M., Poser, I., Rollins, J., Weiland, E. M., and Neugebauer, K. M. 2009. SR protein family members display diverse activities in the formation of nascent and mature mRNPs in vivo. Mol. Cell. 34: 179–190.
  • Sato, H., Hosoda, N., and Maquat, L. E. 2008. Efficiency of the pioneer round of translation affects the cellular site of nonsense-mediated mRNA decay. Mol. Cell. 29: 255–262.
  • Savaldi-Goldstein, S., Aviv, D., Davydov, O., and Fluhr, R. 2003. Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell. 15: 926–938.
  • Savaldi-Goldstein, S., Sessa, G., and Fluhr, R. 2000. The ethylene-inducible PK12 kinase mediates the phosphorylation of SR splicing factors. Plant J. 21: 91–96.
  • Screaton, G. R., Caceres, J. F., Mayeda, A., Bell, M., Plebanski, M., Jackson, D., Bell, J., and Krainer, A. 1995. Identification and characterization of three members of the human SR family of pre‐mRNA splicing factors. EMBO J. 14: 4336–4349.
  • Serpeloni, M., Vidal, N. M., Goldenberg, S., Avila, A. R., and Hoffmann, F. G. 2011. Comparative genomics of proteins involved in RNA nucleocytoplasmic export. BMC Evol. Biol. 11: 7.
  • Shen, H., Kan, J. L., and Green, M. R. 2004. Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Mol. Cell. 13: 367–376.
  • 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.
  • Sinha, R., Allemand, E., Zhang, Z., Karni, R., Myers, M. P., and Krainer, A. R. 2010. Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF. Mol. Cell. Biol. 30: 2762–2774.
  • Sorensen, B. B., Ehrnsberger, H. F., Esposito, S., Pfab, A., Bruckmann, A., Hauptmann, J., Meister, G., Merkl, R., Schubert, T., Langst, G., Melzer, M., Grasser, M., and Grasser, K. D. 2017. The Arabidopsis THO/TREX component TEX1 functionally interacts with MOS11 and modulates mRNA export and alternative splicing events. Plant Mol. Biol. 93: 283–298.
  • Staiger, D. and Brown, J. W. S. 2013. Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell. 25: 3640–3656.
  • Staknis, D. and Reed, R. 1994. SR proteins promote the first specific recognition of Pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex. Mol. Cell. Biol. 14: 7670–7682.
  • Stamm, S. 2008. Regulation of alternative splicing by reversible protein phosphorylation. J. Biol. Chem. 283: 1223–1227.
  • Stankovic, N., Schloesser, M., Joris, M., Sauvage, E., Hanikenne, M., and Motte, P. 2016. Dynamic Distribution and Interaction of the Arabidopsis SRSF1 Subfamily Splicing Factors. Plant Physiol. 170: 1000–1013.
  • Stickeler, E., Kittrell, F., Medina, D., and Berget, S. M. 1999. Stage-specific changes in SR splicing factors and alternative splicing in mammary tumorigenesis. Oncogene 18: 3574–3582.
  • Stork, C. and Zheng, S. 2016. Genome-wide profiling of RNA-Protein Interactions Using CLIP-Seq. Methods Mol. Biol. 1421: 137–151.
  • Sun, Q., Mayeda, A., Hampson, R. K., Krainer, A. R., and Rottman, F. M. 1993. General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev. 7: 2598–2608.
  • Sun, S., Zhang, Z., Sinha, R., Karni, R., and Krainer, A. R. 2010. SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol. 17: 306–312.
  • Sureau, A., Gattoni, R., Dooghe, Y., Stevenin, J., and Soret, J. 2001. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 20: 1785–1796.
  • Tacke, R. and Manley, J. L. 1995. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J. 14: 3540–3551.
  • 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.
  • Terzi, L. C. and Simpson, G. G. 2009. Arabidopsis RNA immunoprecipitation. Plant J. 59: 163–168.
  • Thomas, J., Palusa, S. G., Prasad, K. V., Ali, G. S., Surabhi, G. K., Ben, ‐Hur, A., Abdel, ‐Ghany, S. E., and Reddy, A. S. 2012. Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA. Plant J. 72: 935–946.
  • 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.
  • 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.
  • Tress, M. L., Abascal, F., and Valencia, A. 2017. Most alternative isoforms are not functionally important. Trends Biochem. Sci. 42: 408–410.
  • Ule, J., Jensen, K., Mele, A., and Darnell, R. B. 2005. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37: 376–386.
  • Velazquez-Dones, A., Hagopian, J. C., Ma, C. T., Zhong, X. Y., Zhou, H., Ghosh, G., Fu, X. D., and Adams, J. A. 2005. Mass spectrometric and kinetic analysis of ASF/SF2 phosphorylation by SRPK1 and Clk/Sty. J. Biol. Chem. 280: 41761–41768.
  • Wang, E. T., Sandberg, R., Luo, S. J., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P., and Burge, C. B. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470–476.
  • Wang, J. and Manley, J. L. 1995. Overexpression of the SR proteins ASF/SF2 and SC35 influences alternative splicing in vivo in diverse ways. RNA 1: 335–346.
  • Wang, P., Xue, L., Batelli, G., Lee, S., Hou, Y. J., Van Oosten, M. J., Zhang, H., Tao, W. A., and Zhu, J. K. 2013. Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc. Natl. Acad. Sci. USA. 110: 11205–11210.
  • Wang, Z., Tollervey, J., Briese, M., Turner, D., and Ule, J. 2009. CLIP: construction of cDNA libraries for high-throughput sequencing from RNAs cross-linked to proteins in vivo. Methods 48: 287–293.
  • Will, C. L. and Luhrmann, R. 2011. Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 3: a003707.
  • Wu, H., Sun, S., Tu, K., Gao, Y., Xie, B., Krainer, A. R., and Zhu, J. 2010. A splicing-independent function of SF2/ASF in microRNA processing. Mol. Cell. 38: 67–77.
  • Wu, J. Y. and Maniatis, T. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75: 1061–1070.
  • Xiang, S., Gapsys, V., Kim, H. Y., Bessonov, S., Hsiao, H. H., Mohlmann, S., Klaukien, V., Ficner, R., Becker, S., Urlaub, H., Luhrmann, R., de Groot, B., and Zweckstetter, M. 2013. Phosphorylation drives a dynamic switch in serine/arginine-rich proteins. Structure 21: 2162–2174.
  • Xiao, R., Sun, Y., Ding, J. H., Lin, S., Rose, D. W., Rosenfeld, M. G., Fu, X. D., and Li, X. 2007. Splicing regulator SC35 is essential for genomic stability and cell proliferation during mammalian organogenesis. Mol. Cell. Biol. 27: 5393–5402.
  • Xiao, S. H. and Manley, J. L. 1997. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev. 11: 334–344.
  • Xing, D., Wang, Y., Hamilton, M., Ben-Hur, A., and Reddy, A. S. 2015. Transcriptome-wide identification of RNA targets of Arabidopsis SERINE/ARGININE-RICH45 uncovers the unexpected roles of this RNA binding protein in RNA processing. Plant Cell. 27: 3294–3308.
  • Xu, S., Zhang, Z., Jing, B., Gannon, P., Ding, J., Xu, F., Li, X., and Zhang, Y. 2011. Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLOS Genet. 7: e1002159.
  • Xu, X., Yang, D., Ding, J. H., Wang, W., Chu, P. H., Dalton, N. D., Wang, H. Y., Bermingham, J. R., Ye, Z., Liu, F., Rosenfeld, M. G., Manley, J. L., Ross, J., Chen, J., Xiao, R. P., Cheng, H., and Fu, X. D. 2005. ASF/SF2-regulated CaMKIIdelta alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle. Cell 120: 59–72.
  • Yan, Q., Xia, X., Sun, Z., and Fang, Y. 2017. Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes. PLOS Genet. 13: e1006663.
  • Yeakley, J. M., Tronchere, H., Olesen, J., Dyck, J. A., Wang, H. Y., and Fu, X. D. 1999. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors. J. Cell Biol. 145: 447–455.
  • Yoon, E. K., Krishnamurthy, P., Kim, J. A., Jeong, M. J., and Lee, S. I. 2018. Genome-wide characterization of Brassica rapa genes encoding serine/arginine-rich proteins: expression and alternative splicing events by abiotic stresses. J. Plant Biol. 61: 198–209.
  • Yu, H., Tian, C., Yu, Y., and Jiao, Y. 2016. Transcriptome survey of the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana. Mol. Plant. 9: 749–752.
  • Yun, C. Y., Velazquez-Dones, A. L., Lyman, S. K., and Fu, X. D. 2003. Phosphorylation-dependent and -independent nuclear import of RS domain-containing splicing factors and regulators. J. Biol. Chem. 278: 18050–18055.
  • Zahler, A. M., Lane, W. S., Stolk, J. A., and Roth, M. B. 1992. SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 6: 837–847.
  • Zahler, A. M., Neugebauer, K. M., Lane, W. S., and Roth, M. B. 1993. Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260: 219–222.
  • Zahler, A. M. and Roth, M. B. 1995. Distinct functions of SR proteins in recruitment of U1 small nuclear ribonucleoprotein to alternative 5' splice sites. Proc. Natl. Acad. Sci. USA. 92: 2642–2646.
  • Zhang, P., Deng, H., Xiao, F., and Liu, Y. 2013. Alterations of alternative splicing patterns of Ser/Arg-rich (SR) genes in response to hormones and stresses treatments in different ecotypes of rice (Oryza sativa). J. Integr. Agric. 12: 737–748.
  • Zhang, W., Du, B., Liu, D., and Qi, X. 2014a. Splicing factor SR34b mutation reduces cadmium tolerance in Arabidopsis by regulating iron-regulated transporter 1 gene. Biochem. Biophys. Res. Commun. 455: 312–317.
  • Zhang, W. J. and Wu, J. Y. 1996. Functional properties of p54, a novel SR protein active in constitutive and alternative splicing. Mol. Cell. Biol. 16: 5400–5408.
  • Zhang, X. N., Mo, C., Garrett, W. M., and Cooper, B. 2014b. Phosphothreonine 218 is required for the function of SR45.1 in regulating flower petal development in Arabidopsis. Plant Signal Behav. 9: e29134.
  • 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.
  • Zhang, X. N., Shi, Y., Powers, J. J., Gowda, N. B., Zhang, C., Ibrahim, H. M., Ball, H. B., Chen, S. L., Lu, H., and Mount, S. M. 2017. Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana. BMC Genomics. 18: 772.
  • Zhang, Z. and Krainer, A. R. 2004. Involvement of SR proteins in mRNA surveillance. Mol. Cell. 16: 597–607.
  • Zhong, X. Y., Ding, J. H., Adams, J. A., Ghosh, G., and Fu, X. D. 2009a. Regulation of SR protein phosphorylation and alternative splicing by modulating kinetic interactions of SRPK1 with molecular chaperones. Genes Dev. 23: 482–495.
  • Zhong, X. Y., Wang, P., Han, J., Rosenfeld, M. G., and Fu, X. D. 2009b. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell. 35: 1–10.
  • Zhou, Z. and Fu, X. D. 2013. Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122: 191–207.
  • Zhou, Z., Qiu, J., Liu, W., Zhou, Y., Plocinik, R. M., Li, H., Hu, Q., Ghosh, G., Adams, J. A., Rosenfeld, M. G., and Fu, X. D. 2012. The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol. Cell. 47: 422–433.
  • Zhu, F. Y., Chen, M. X., Ye, N. H., Shi, L., Ma, K. L., Yang, J. F., Cao, Y. Y., Zhang, Y. J., Yoshida, T., Fernie, A. R., Fan, G. Y., Wen, B., Zhou, R., Liu, T. Y., Fan, T., Gao, B., Zhang, D., Hao, G. F., Xiao, S., Liu, Y. G., and Zhang, J. H. 2017. Proteogenomic analysis reveals alternative splicing and translation as part of the abscisic acid response in Arabidopsis seedlings. Plant J. 91: 518–533.
  • Zhu, J. and Krainer, A. R. 2000. Pre-mRNA splicing in the absence of an SR protein RS domain. Genes Dev. 14: 3166–3178.
  • Zuo, P. and Manley, J. L. 1993. Functional domains of the human splicing factor ASF/SF2. EMBO J. 12: 4727–4737.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.