Table of Contents
Advances in Botany
Volume 2015, Article ID 419428, 13 pages
http://dx.doi.org/10.1155/2015/419428
Review Article

Shaping the Arabidopsis Transcriptome through Alternative Splicing

Molecular Cell Physiology, Faculty of Biology, Bielefeld University, Universitaetsstrasse 25, 33615 Bielefeld, Germany

Received 16 November 2014; Accepted 17 January 2015

Academic Editor: Tomotsugu Koyama

Copyright © 2015 Dorothee Staiger. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. J. Moore, “From birth to death: the complex lives of eukaryotic mRNAs,” Science, vol. 309, no. 5740, pp. 1514–1518, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Cheng and X. Chen, “Posttranscriptional control of plant development,” Current Opinion in Plant Biology, vol. 7, no. 1, pp. 20–25, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. Z. J. Lorković, “Role of plant RNA-binding proteins in development, stress response and genome organization,” Trends in Plant Science, vol. 14, no. 4, pp. 229–236, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Rataj and G. G. Simpson, “Message ends: RNA 3′ processing and flowering time control,” Journal of Experimental Botany, vol. 65, no. 2, pp. 353–363, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. G. G. Simpson, “The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time,” Current Opinion in Plant Biology, vol. 7, no. 5, pp. 570–574, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Staiger and R. Green, “RNA-based regulation in the plant circadian clock,” Trends in Plant Science, vol. 16, no. 10, pp. 517–523, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Staiger, C. Korneli, M. Lummer, and L. Navarro, “Emerging role for RNA-based regulation in plant immunity,” New Phytologist, vol. 197, no. 2, pp. 394–404, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. R. F. Carvalho, C. V. Feijão, and P. Duque, “On the physiological significance of alternative splicing events in higher plants,” Protoplasma, vol. 250, no. 3, pp. 639–650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. M. Berget, C. Moore, and P. A. Sharp, “Spliced segments at the 5′ terminus of adenovirus 2 late mRNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 8, pp. 3171–3175, 1977. View at Publisher · View at Google Scholar · View at Scopus
  10. L. T. Chow, R. E. Gelinas, T. R. Broker, and R. J. Roberts, “An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA,” Cell, vol. 12, no. 1, pp. 1–8, 1977. View at Publisher · View at Google Scholar · View at Scopus
  11. P. A. Sharp, “Split genes and RNA splicing,” Cell, vol. 77, no. 6, pp. 805–815, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Gilbert, “Why genes in pieces?” Nature, vol. 271, no. 5645, article 501, 1978. View at Publisher · View at Google Scholar · View at Scopus
  13. D. L. Black, “Mechanisms of alternative pre-messenger RNA splicing,” Annual Review of Biochemistry, vol. 72, pp. 291–336, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. C. W. J. Smith, J. G. Patton, and B. Nadal-Ginard, “Alternative splicing in the control of gene expression,” Annual Review of Genetics, vol. 23, pp. 527–577, 1989. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Braunschweig, S. Gueroussov, A. M. Plocik, B. R. Graveley, and B. J. Blencowe, “Dynamic integration of splicing within gene regulatory pathways,” Cell, vol. 152, no. 6, pp. 1252–1269, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. T. W. Nilsen and B. R. Graveley, “Expansion of the eukaryotic proteome by alternative splicing,” Nature, vol. 463, no. 7280, pp. 457–463, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. A. S. N. Reddy, Y. Marquez, M. Kalyna, and A. Barta, “Complexity of the alternative splicing landscape in plants,” Plant Cell, vol. 25, no. 10, pp. 3657–3683, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. B.-B. Wang and V. Brendel, “Genomewide comparative analysis of alternative splicing in plants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7175–7180, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. W. B. Barbazuk, Y. Fu, and K. M. McGinnis, “Genome-wide analyses of alternative splicing in plants: opportunities and challenges,” Genome Research, vol. 18, no. 9, pp. 1381–1392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. A. Filichkin, G. Breton, H. D. Priest et al., “Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules,” PLoS ONE, vol. 6, no. 6, Article ID e16907, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Arciga-Reyes, L. Wootton, M. Kieffer, and B. Davies, “UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis,” Plant Journal, vol. 47, no. 3, pp. 480–489, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. O. Isken and L. E. Maquat, “The multiple lives of NMD factors: balancing roles in gene and genome regulation,” Nature Reviews Genetics, vol. 9, no. 9, pp. 699–712, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Nicholson and O. Mühlemann, “Cutting the nonsense: the degradation of PTC-containing mRNAs,” Biochemical Society Transactions, vol. 38, no. 6, pp. 1615–1620, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. M. W. Hentze and A. E. Kulozik, “A perfect message: RNA surveillance and nonsense-mediated decay,” Cell, vol. 96, no. 3, pp. 307–310, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. L. E. Maquat, “Nonsense-mediated mRNA decay,” Current Biology, vol. 12, no. 6, pp. R196–R197, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. N. J. McGlincy and C. W. J. Smith, “Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense?” Trends in Biochemical Sciences, vol. 33, no. 8, pp. 385–393, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Heintzen, S. Melzer, R. Fischer, S. Kappeler, K. Apel, and D. Staiger, “A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue,” Plant Journal, vol. 5, no. 6, pp. 799–813, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Ner-Gaon, R. Halachmi, S. Savaldi-Goldstein, E. Rubin, R. Ophir, and R. Fluhr, “Intron retention is a major phenomenon in alternative splicing in Arabidopsis,” Plant Journal, vol. 39, no. 6, pp. 877–885, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Zhu, S. D. Schlueter, and V. Brendel, “Refined annotation of the Arabidopsis genome by complete expressed sequence tag mapping,” Plant Physiology, vol. 132, no. 2, pp. 469–484, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Menges, L. Hennig, W. Gruissem, and J. A. H. Murray, “Genome-wide gene expression in an Arabidopsis cell suspension,” Plant Molecular Biology, vol. 53, no. 4, pp. 423–442, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. S. P. Hazen and S. A. Kay, “Gene arrays are not just for measuring gene expression,” Trends in Plant Science, vol. 8, no. 9, pp. 413–416, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. C. G. Simpson, J. Fuller, M. Maronova et al., “Monitoring changes in alternative precursor messenger RNA splicing in multiple gene transcripts,” Plant Journal, vol. 53, no. 6, pp. 1035–1048, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. K. D. Raczynska, C. G. Simpson, A. Ciesiolka et al., “Involvement of the nuclear cap-binding protein complex in alternative splicing in Arabidopsis thaliana,” Nucleic Acids Research, vol. 38, no. 1, Article ID gkp869, pp. 265–278, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. S. E. Sanchez, E. Petrillo, E. J. Beckwith et al., “A methyl transferase links the circadian clock to the regulation of alternative splicing,” Nature, vol. 468, no. 7320, pp. 112–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Kalyna, C. G. Simpson, N. H. Syed et al., “Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis,” Nucleic Acids Research, vol. 40, no. 6, pp. 2454–2469, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Streitner, C. G. Simpson, P. Shaw, S. Danisman, J. W. S. Brown, and D. Staiger, “Small changes in ambient temperature affect alternative splicing in Arabidopsis thaliana,” Plant Signaling and Behavior, vol. 8, no. 7, Article ID e24638, 2013. View at Google Scholar · View at Scopus
  37. A. B. James, N. H. Syed, S. Bordage et al., “Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes,” Plant Cell, vol. 24, no. 3, pp. 961–981, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. C. G. Simpson, D. Lewandowska, M. Liney et al., “Arabidopsis PTB1 and PTB2 proteins negatively regulate splicing of a mini-exon splicing reporter and affect alternative splicing of endogenous genes differentially,” New Phytologist, vol. 203, pp. 424–436, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. S. A. Filichkin, H. D. Priest, S. A. Givan et al., “Genome-wide mapping of alternative splicing in Arabidopsis thaliana,” Genome Research, vol. 20, no. 1, pp. 45–58, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Marquez, J. W. S. Brown, C. G. Simpson, A. Barta, and M. Kalyna, “Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis,” Genome Research, vol. 22, no. 6, pp. 1184–1195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Rühl, E. Stauffer, A. Kahles et al., “Polypyrimidine tract binding protein homologs from Arabidopsis are key regulators of alternative splicing with implications in fundamental developmental processes,” Plant Cell, vol. 24, no. 11, pp. 4360–4375, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. A. S. N. Reddy, “Alternative splicing of pre-messenger RNAs in plants in the genomic era,” Annual Review of Plant Biology, vol. 58, pp. 267–294, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. E. T. Wang, R. Sandberg, S. Luo et al., “Alternative isoform regulation in human tissue transcriptomes,” Nature, vol. 456, no. 7221, pp. 470–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. G. S. Ali and A. S. N. Reddy, “Regulation of alternative splicing of pre-mRNAs by stresses,” Current Topics in Microbiology and Immunology, vol. 326, pp. 257–275, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Kazan, “Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged,” Trends in Plant Science, vol. 8, no. 10, pp. 468–471, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Staiger and J. W. S. Brown, “Alternative splicing at the intersection of biological timing, development, and stress responses,” Plant Cell, vol. 25, no. 10, pp. 3640–3656, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. S. P. Dinesh-Kumar and B. J. Baker, “Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 4, pp. 1908–1913, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. X.-C. Zhang and W. Gassmann, “Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses,” Plant Physiology, vol. 145, no. 4, pp. 1577–1587, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Rogers and X. Chen, “Biogenesis, turnover, and mode of action of plant microRNAs,” Plant Cell, vol. 25, no. 7, pp. 2383–2399, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. C. L. Will and R. Lührmann, “Spliceosome structure and function,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 7, Article ID a003707, pp. 1–2, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. M. C. Wahl, C. L. Will, and R. Lührmann, “The spliceosome: design principles of a dynamic RNP machine,” Cell, vol. 136, no. 4, pp. 701–718, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Gabut, S. Chaudhry, and B. J. Blencowe, “SnapShot: the splicing regulatory machinery,” Cell, vol. 133, no. 1, pp. 192–192.e1, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Tharun, “Roles of eukaryotic Lsm proteins in the regulation of mRNA function,” International Review of Cell and Molecular Biology, vol. 272, pp. 149–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. G. B. Gonsalvez, T. K. Rajendra, L. Tian, and A. G. Matera, “The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance,” Current Biology, vol. 16, no. 11, pp. 1077–1089, 2006. View at Publisher · View at Google Scholar
  55. J. W. S. Brown, G. Feix, and D. Frendewey, “Accurate in vitro splicing of two pre-mRNA plant introns in a HeLa cell nuclear extract,” The EMBO Journal, vol. 5, no. 11, pp. 2749–2758, 1986. View at Google Scholar · View at Scopus
  56. A. Barta, K. Sommergruber, D. Thompson, K. Hartmuth, M. A. Matzke, and A. J. M. Matzke, “The expression of a nopaline synthase—human growth hormone chimaeric gene in transformed tobacco and sunflower callus tissue,” Plant Molecular Biology, vol. 6, no. 5, pp. 347–357, 1986. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Wiebauer, J. J. Herrero, and W. Filipowicz, “Nuclear pre-mRNA processing in plants: distinct modes of 3′-splice-site selection in plants and animals,” Molecular and Cellular Biology, vol. 8, no. 5, pp. 2042–2051, 1988. View at Google Scholar · View at Scopus
  58. H. Iwata and O. Gotoh, “Comparative analysis of information contents relevant to recognition of introns in many species,” BMC Genomics, vol. 12, article 45, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. J. W. Brown, C. G. Simpson, G. Thow et al., “Splicing signals and factors in plant intron removal,” Biochemical Society Transactions, vol. 30, no. 2, pp. 146–149, 2002. View at Google Scholar · View at Scopus
  60. S. Schwartz, E. Meshorer, and G. Ast, “Chromatin organization marks exon-intron structure,” Nature Structural and Molecular Biology, vol. 16, no. 9, pp. 990–995, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. B.-B. Wang and V. Brendel, “The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing,” Genome Biology, vol. 5, article R102, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Koncz, F. deJong, N. Villacorta, D. Szakonyi, and Z. Koncz, “The spliceosome-activating complex: molecular mechanisms underlying the function of a pleiotropic regulator,” Frontiers in Plant Science, vol. 3, article 9, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Chen and J. L. Manley, “Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches,” Nature Reviews Molecular Cell Biology, vol. 10, no. 11, pp. 741–754, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Barta, M. Kalyna, and A. S. N. Reddy, “Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants,” Plant Cell, vol. 22, no. 9, pp. 2926–2929, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Lopato, A. Mayeda, A. R. Krainer, and A. Barta, “Pre-mRNA splicing in plants: characterization of Ser/Arg splicing factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 7, pp. 3074–3079, 1996. View at Publisher · View at Google Scholar · View at Scopus
  66. A. S. Reddy, I. S. Day, J. Gohring, and A. Barta, “Localization and dynamics of plant splicing regulators,” Plant Physiology, vol. 158, pp. 67–77, 2012. View at Google Scholar
  67. M. Kalyna and A. Barta, “A plethora of plant serine/arginine-rich proteins: redundancy or evolution of novel gene functions?” Biochemical Society Transactions, vol. 32, no. 4, pp. 561–564, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Kalyna, S. Lopato, and A. Barta, “Ectopic expression of atRSZ33 reveals its function in splicing and causes pleiotropic changes in development,” Molecular Biology of the Cell, vol. 14, no. 9, pp. 3565–3577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Lopato, M. Kalyna, S. Dorner, R. Kobayashi, A. R. Krainer, and A. Barta, “atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes,” Genes and Development, vol. 13, no. 8, pp. 987–1001, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. E. Petrillo, M. A. Godoy Herz, A. Fuchs et al., “A chloroplast retrograde signal regulates nuclear alternative splicing,” Science, vol. 344, no. 6182, pp. 427–430, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. G. Lazar and H. M. Goodman, “The Arabidopsis splicing factor SR1 is regulated by alternative splicing,” Plant Molecular Biology, vol. 42, no. 4, pp. 571–581, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Golovkin and A. S. N. Reddy, “The plant U1 small nuclear ribonucleoprotein particle 70k protein interacts with two novel serine/arginine-rich proteins,” Plant Cell, vol. 10, no. 10, pp. 1637–1648, 1998. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Lopato, E. Waigmann, and A. Barta, “Characterization of a novel arginine/serine-rich splicing factor in Arabidopsis,” Plant Cell, vol. 8, no. 12, pp. 2255–2264, 1996. View at Publisher · View at Google Scholar · View at Scopus
  74. S. G. Palusa and A. S. N. Reddy, “Extensive coupling of alternative splicing of pre-mRNAs of serine/arginine (SR) genes with nonsense-mediated decay,” New Phytologist, vol. 185, no. 1, pp. 83–89, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. K. Iida and M. Go, “Survey of conserved alternative splicing events of mRNAs encoding SR proteins in land plants,” Molecular Biology and Evolution, vol. 23, no. 5, pp. 1085–1094, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Kalyna, S. Lopato, V. Voronin, and A. Barta, “Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins,” Nucleic Acids Research, vol. 34, no. 16, pp. 4395–4405, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Thomas, S. G. Palusa, K. V. S. K. Prasad et al., “Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA,” Plant Journal, vol. 72, no. 6, pp. 935–946, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Tanabe, A. Kimura, K. Yoshimura, and S. Shigeoka, “Plant-specific SR-related protein atSR45a interacts with spliceosomal proteins in plant nucleus,” Plant Molecular Biology, vol. 70, no. 3, pp. 241–252, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. I. S. Day, M. Golovkin, S. G. Palusa et al., “Interactions of SR45, an SR-like protein, with spliceosomal proteins and an intronic sequence: insights into regulated splicing,” The Plant Journal, vol. 71, no. 6, pp. 936–947, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. G. S. Ali, S. G. Palusa, M. Golovkin, J. Prasad, J. L. Manley, and A. S. N. Reddy, “Regulation of plant developmental processes by a novel splicing factor,” PLoS ONE, vol. 2, no. 5, article e471, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. X.-N. Zhang and S. M. Mount, “Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development,” Plant Physiology, vol. 150, no. 3, pp. 1450–1458, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. R. F. Carvalho, S. D. Carvalho, and P. Duque, “The Plant-Specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis,” Plant Physiology, vol. 154, no. 2, pp. 772–783, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Wachter, C. Rühl, and E. Stauffer, “The role of polypyrimidine tract-binding proteins and other hnRNP proteins in plant splicing regulation,” Frontiers in Plant Science, vol. 3, article 81, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. R. Martinez-Contreras, P. Cloutier, L. Shkreta, J.-F. Fisette, T. Revil, and B. Chabot, “hnRNP proteins and splicing control,” Advances in Experimental Medicine and Biology, vol. 623, pp. 123–147, 2007. View at Google Scholar · View at Scopus
  85. J. M. Izquierdo, N. Majós, S. Bonnal et al., “Regulation of fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition,” Molecular Cell, vol. 19, no. 4, pp. 475–484, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. P. L. Boutz, P. Stoilov, Q. Li et al., “A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons,” Genes and Development, vol. 21, no. 13, pp. 1636–1652, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. E. Stauffer, A. Westermann, G. Wagner, and A. Wachter, “Polypyrimidine tract-binding protein homologues from Arabidopsis underlie regulatory circuits based on alternative splicing and downstream control,” The Plant Journal, vol. 64, no. 2, pp. 243–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. D. Staiger, L. Zecca, D. A. Wieczorek Kirk, K. Apel, and L. Eckstein, “The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA,” Plant Journal, vol. 33, no. 2, pp. 361–371, 2003. View at Publisher · View at Google Scholar · View at Scopus
  89. J. C. Schöning, C. Streitner, D. R. Page et al., “Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation,” Plant Journal, vol. 52, no. 6, pp. 1119–1130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. J. S. Kim, S. J. Park, K. J. Kwak et al., “Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli,” Nucleic Acids Research, vol. 35, no. 2, pp. 506–516, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Schüttpelz, J. C. Schöning, S. Doose et al., “Changes in conformational dynamics of mRNA upon AtGRP7 binding studied by fluorescence correlation spectroscopy,” Journal of the American Chemical Society, vol. 130, no. 29, pp. 9507–9513, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Fuhrmann, J. C. Schoening, D. Anselmetti, D. Staiger, and R. Ros, “Quantitative analysis of single-molecule RNA-protein interaction,” Biophysical Journal, vol. 96, no. 12, pp. 5030–5039, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Izaurralde, A. Jarmolowski, C. Beisel, I. W. Mattaj, G. Dreyfuss, and U. Fischer, “A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export,” The Journal of Cell Biology, vol. 137, pp. 27–35, 1997. View at Publisher · View at Google Scholar
  94. M. C. Siomi, P. S. Eder, N. Kataoka, L. Wan, Q. Liu, and G. Dreyfuss, “Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins,” Journal of Cell Biology, vol. 138, no. 6, pp. 1181–1192, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. H. Siomi and G. Dreyfuss, “A nuclear localization domain in the hnRNP A1 protein,” The Journal of Cell Biology, vol. 129, no. 3, pp. 551–560, 1995. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Lummer, F. Humpert, C. Steuwe et al., “Reversible photoswitchable DRONPA-s monitors nucleocytoplasmic transport of an RNA-binding protein in transgenic plants,” Traffic, vol. 12, no. 6, pp. 693–702, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Ziemienowicz, D. Haasen, D. Staiger, and T. Merkle, “Arabidopsis transportin1 is the nuclear import receptor for the circadian clock-regulated RNA-binding protein AtGRP7,” Plant Molecular Biology, vol. 53, no. 1-2, pp. 201–212, 2003. View at Publisher · View at Google Scholar · View at Scopus
  98. V. Leder, M. Lummer, K. Tegeler et al., “Mutational definition of binding requirements of an hnRNP-like protein in Arabidopsis using fluorescence correlation spectroscopy,” Biochemical and Biophysical Research Communications, vol. 453, no. 1, pp. 69–74, 2014. View at Publisher · View at Google Scholar
  99. C. D. Carpenter, J. A. Kreps, and A. E. Simon, “Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm,” Plant Physiology, vol. 104, no. 3, pp. 1015–1025, 1994. View at Publisher · View at Google Scholar · View at Scopus
  100. D. Staiger and C. Heintzen, “The circadian system of Arabidopsis thaliana: forward and reverse genetic approaches,” Chronobiology International, vol. 16, no. 1, pp. 1–16, 1999. View at Publisher · View at Google Scholar · View at Scopus
  101. J. C. Schöning, C. Streitner, I. M. Meyer, Y. Gao, and D. Staiger, “Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis,” Nucleic Acids Research, vol. 36, no. 22, pp. 6977–6987, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. C. Streitner, L. Hennig, C. Korneli, and D. Staiger, “Global transcript profiling of transgenic plants constitutively overexpressing the RNA-binding protein AtGRP7,” BMC Plant Biology, vol. 10, article 221, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. B. Löhr, C. Streitner, A. Steffen, T. Lange, and D. Staiger, “A glycine-rich RNA-binding protein affects gibberellin biosynthesis in Arabidopsis,” Molecular Biology Reports, vol. 41, no. 1, pp. 439–445, 2014. View at Publisher · View at Google Scholar · View at Scopus
  104. C. Schmal, P. Reimann, and D. Staiger, “A circadian clock-regulated toggle switch explains AtGRP7 and AtGRP8 oscillations in Arabidopsis thaliana,” PLoS Computational Biology, vol. 9, no. 3, Article ID e1002986, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Streitner, T. Köster, C. G. Simpson et al., “An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana,” Nucleic Acids Research, vol. 40, no. 22, pp. 11240–11255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. T. Köster and D. Staiger, “RNA-binding protein immunoprecipitation from whole-cell extracts,” Methods in Molecular Biology, vol. 1062, pp. 679–695, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. Z. Q. Fu, M. Guo, B.-R. Jeong et al., “A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity,” Nature, vol. 447, no. 7142, pp. 284–288, 2007. View at Publisher · View at Google Scholar · View at Scopus
  108. B.-R. Jeong, Y. Lin, A. Joe et al., “Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity,” The Journal of Biological Chemistry, vol. 286, no. 50, pp. 43272–43281, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. V. Nicaise, A. Joe, B.-R. Jeong et al., “Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7,” EMBO Journal, vol. 32, no. 5, pp. 701–712, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. C. Hackmann, C. Korneli, M. Kutyniok et al., “Salicylic acid-dependent and -independent impact of an RNA-binding protein on plant immunity,” Plant, Cell and Environment, vol. 37, no. 3, pp. 696–706, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Golisz, P. J. Sikorski, K. Kruszka, and J. Kufel, “Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation,” Nucleic Acids Research, vol. 41, no. 12, pp. 6232–6249, 2013. View at Publisher · View at Google Scholar · View at Scopus
  112. P. Cui, S. Zhang, F. Ding, S. Ali, and L. Xiong, “Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis,” Genome Biology, vol. 15, no. 1, article R1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. Z. Zhang, S. Zhang, Y. Zhang et al., “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, vol. 23, no. 1, pp. 396–411, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. B.-H. Lee, A. Kapoor, J. Zhu, and J.-K. Zhu, “STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis,” Plant Cell, vol. 18, no. 7, pp. 1736–1749, 2006. View at Publisher · View at Google Scholar · View at Scopus
  115. R. Hogg, J. C. McGrail, and R. T. O'Keefe, “The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing,” Biochemical Society Transactions, vol. 38, no. 4, pp. 1110–1115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. Y. Zhang, S. Goritschnig, X. Dong, and X. Li, “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, vol. 15, no. 11, pp. 2636–2646, 2003. View at Publisher · View at Google Scholar · View at Scopus
  117. K. Palma, Q. Zhao, Y. T. Cheng et al., “Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms,” Genes and Development, vol. 21, no. 12, pp. 1484–1493, 2007. View at Publisher · View at Google Scholar · View at Scopus
  118. J. Monaghan, F. Xu, M. Gao et al., “Two Prp19-like U-box proteins in the MOS4-associated complex play redundant roles in plant innate immunity,” PLoS Pathogens, vol. 5, no. 7, Article ID e1000526, 2009. View at Publisher · View at Google Scholar · View at Scopus
  119. F. Xu, S. Xu, M. Wiermer, Y. Zhang, and X. Li, “The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes,” Plant Journal, vol. 70, no. 6, pp. 916–928, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. J. Monaghan, F. Xu, S. Xu, Y. Zhang, and X. Li, “Two putative RNA-binding proteins function with unequal genetic redundancy in the MOS4-associated complex,” Plant Physiology, vol. 154, no. 4, pp. 1783–1793, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. N. Rasche, O. Dybkov, J. Schmitzová, B. Akyildiz, P. Fabrizio, and R. Lührmann, “Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre,” EMBO Journal, vol. 31, no. 6, pp. 1591–1604, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. M. Ohtani, T. Demura, and M. Sugiyama, “Arabidopsis root initiation defective1, a DEAH-box RNA helicase involved in pre-mrna splicing, is essential for plant development,” The Plant Cell, vol. 25, no. 6, pp. 2056–2069, 2013. View at Publisher · View at Google Scholar · View at Scopus
  123. M. A. Jones, B. A. Williams, J. McNicol, C. G. Simpson, J. W. S. Brown, and S. L. Harmer, “Mutation of Arabidopsis SPLICEOSOMAL TIMEKEEPER LOCUS1 causes circadian clock defects,” The Plant Cell, vol. 24, pp. 4907–4916, 2012. View at Google Scholar
  124. X. Wang, F. Wu, Q. Xie et al., “SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis,” The Plant Cell, vol. 24, no. 8, pp. 3278–3295, 2012. View at Publisher · View at Google Scholar · View at Scopus
  125. S. Laubinger, T. Sachsenberg, G. Zeller et al., “Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 25, pp. 8795–8800, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. K. D. Raczynska, A. Stepien, D. Kierzkowski et al., “The SERRATE protein is involved in alternative splicing in Arabidopsis thaliana,” Nucleic Acids Research, vol. 42, no. 2, pp. 1224–1244, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. S. Hong, H.-R. Songa, K. Lutz, R. A. Kerstetterc, T. P. Michael, and C. R. McClung, “Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 49, pp. 21211–21216, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. X. Deng, L. Gu, C. Liu et al., “Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 44, pp. 19114–19119, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. S. de la Fuente van Bentem, D. Anrather, E. Roitinger et al., “Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism,” Nucleic Acids Research, vol. 34, no. 11, pp. 3267–3278, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. T. Feilner, C. Hultschig, J. Lee et al., “High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates,” Molecular and Cellular Proteomics, vol. 4, no. 10, pp. 1558–1568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. S. Savaldi-Goldstein, D. Aviv, O. Davydov, and R. Fluhr, “Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression,” Plant Cell, vol. 15, no. 4, pp. 926–938, 2003. View at Publisher · View at Google Scholar · View at Scopus
  132. G. Drechsel, A. Kahles, A. K. Kesarwani et al., “Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome,” The Plant Cell, vol. 25, no. 10, pp. 3726–3742, 2013. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Z. Ni, L. Grate, J. P. Donohue et al., “Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay,” Genes and Development, vol. 21, no. 6, pp. 708–718, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. L. F. Lareau, M. Inada, R. E. Green, J. C. Wengrod, and S. E. Brenner, “Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements,” Nature, vol. 446, no. 7138, pp. 926–929, 2007. View at Publisher · View at Google Scholar · View at Scopus
  135. J. Göhring, J. Jacak, and A. Barta, “Imaging of endogenous messenger RNA splice variants in living cells reveals nuclear retention of transcripts inaccessible to nonsense-mediated decay in Arabidopsis,” The Plant Cell, vol. 26, no. 2, pp. 754–764, 2014. View at Publisher · View at Google Scholar · View at Scopus
  136. N. Zhang, R. P. Kallis, R. G. Ewy, and A. R. Portis Jr., “Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 5, pp. 3330–3334, 2002. View at Publisher · View at Google Scholar · View at Scopus
  137. A. Sugio, R. Dreos, F. Aparicio, and A. J. Maule, “The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis,” The Plant Cell, vol. 21, no. 2, pp. 642–654, 2009. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Liu, N. Sun, M. Liu, B. Du, X. Wang, and X. Qi, “An autoregulatory loop controlling ArabidopsisHsfA2 expression: role of heat shock-induced alternative splicing,” Plant Physiology, vol. 162, no. 1, pp. 512–521, 2013. View at Publisher · View at Google Scholar · View at Scopus
  139. H. S. Chung, T. F. Cooke, C. L. Depew et al., “Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling,” Plant Journal, vol. 63, no. 4, pp. 613–622, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. J. E. Moreno, C. Shyu, M. L. Campos et al., “Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10,” Plant Physiology, vol. 162, no. 2, pp. 1006–1017, 2013. View at Publisher · View at Google Scholar · View at Scopus
  141. M. Hiller, K. Huse, K. Szafranski et al., “Widespread occurrence of alternative splicing at NAGNAG acceptors contributes to proteome plasticity,” Nature Genetics, vol. 36, pp. 1255–1257, 2004. View at Google Scholar
  142. K. Iida, M. Shionyu, and Y. Suso, “Alternative splicing at NAGNAG acceptor sites shares common properties in land plants and mammals,” Molecular Biology and Evolution, vol. 25, no. 4, pp. 709–718, 2008. View at Publisher · View at Google Scholar · View at Scopus
  143. S. Schindler, K. Szafranski, M. Hiller et al., “Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related protein-coding genes,” BMC Genomics, vol. 9, article 159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  144. V. Kriechbaumer, P. Wang, C. Hawes, and B. M. Abell, “Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation,” The Plant Journal, vol. 70, no. 2, pp. 292–302, 2012. View at Publisher · View at Google Scholar · View at Scopus
  145. Y. Nagashima, K.-I. Mishiba, E. Suzuki, Y. Shimada, Y. Iwata, and N. Koizumi, “Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor,” Scientific Reports, vol. 1, article 29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. E. Remy, T. R. Cabrito, P. Baster et al., “A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis,” The Plant Cell, vol. 25, no. 3, pp. 901–926, 2013. View at Publisher · View at Google Scholar · View at Scopus
  147. T. Jayaweera, C. Siriwardana, S. Dharmasiri et al., “Alternative splicing of Arabidopsis IBR5 pre-mRNA generates two IBR5 isoforms with distinct and overlapping functions,” PLoS ONE, vol. 9, no. 8, Article ID e102301, 2014. View at Publisher · View at Google Scholar
  148. E. Remy, T. R. Cabrito, R. A. Batista et al., “Intron retention in the 5'UTR of the novel ZIF2 transporter enhances translation to promote zinc tolerance in Arabidopsis,” PLoS Genetics, vol. 10, no. 5, Article ID e1004375, 2014. View at Publisher · View at Google Scholar · View at Scopus
  149. G. J. Goodall and W. Filipowicz, “Different effects of intron nucleotide composition and secondary structure on pre-mRNA splicing in monocot and dicot plants,” EMBO Journal, vol. 10, no. 9, pp. 2635–2644, 1991. View at Google Scholar · View at Scopus
  150. S. Bocobza, A. Adato, T. Mandel, M. Shapira, E. Nudler, and A. Aharoni, “Riboswitch-dependent gene regulation and its evolution in the plant kingdom,” Genes and Development, vol. 21, no. 22, pp. 2874–2879, 2007. View at Publisher · View at Google Scholar · View at Scopus
  151. A. Wachter, M. Tunc-Ozdemir, B. C. Grove, P. J. Green, D. K. Shintani, and R. R. Breaker, “Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs,” Plant Cell, vol. 19, no. 11, pp. 3437–3450, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. M. C. Hammond, A. Wachter, and R. R. Breaker, “A plant 5S ribosomal RNA mimic regulates alternative splicing of transcription factor IIIA pre-mRNAs,” Nature Structural and Molecular Biology, vol. 16, no. 5, pp. 541–549, 2009. View at Publisher · View at Google Scholar · View at Scopus
  153. Y. Fu, O. Bannach, H. Chen et al., “Alternative splicing of anciently exonized 5S rRNA regulates plant transcription factor TFIIIA,” Genome Research, vol. 19, no. 5, pp. 913–921, 2009. View at Publisher · View at Google Scholar · View at Scopus
  154. F. Bardou, F. Ariel, C. G. Simpson et al., “Long noncoding RNA modulates alternative splicing regulators in arabidopsis,” Developmental Cell, vol. 30, no. 2, pp. 166–176, 2014. View at Publisher · View at Google Scholar
  155. I. M. Silverman, F. Li, and B. D. Gregory, “Genomic era analyses of RNA secondary structure and RNA-binding proteins reveal their significance to post-transcriptional regulation in plants,” Plant Science, vol. 205-206, pp. 55–62, 2013. View at Publisher · View at Google Scholar · View at Scopus
  156. X. Yang, H. Zhang, and L. Li, “Alternative mRNA processing increases the complexity of microRNA-based gene regulation in Arabidopsis,” The Plant Journal, vol. 70, no. 3, pp. 421–431, 2012. View at Publisher · View at Google Scholar · View at Scopus
  157. G. Wu, M. Y. Park, S. R. Conway, J.-W. Wang, D. Weigel, and R. S. Poethig, “The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis,” Cell, vol. 138, no. 4, pp. 750–759, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. G. Wu and R. S. Poethig, “Temporal regulation of shoot development in Arabidopsis thaliana by miRr156 and its target SPL3,” Development, vol. 133, no. 18, pp. 3539–3547, 2006. View at Publisher · View at Google Scholar · View at Scopus
  159. Y. Meng, C. Shao, X. Ma, and H. Wang, “Introns targeted by plant microRNAs: a possible novel mechanism of gene regulation,” Rice, vol. 6, no. 1, pp. 1–10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  160. Z. Szweykowska-Kulinska, A. Jarmolowski, and F. Vazquez, “The crosstalk between plant microRNA biogenesis factors and the spliceosome,” Plant Signaling and Behavior, vol. 8, no. 11, Article ID e26955, 2013. View at Publisher · View at Google Scholar · View at Scopus
  161. J. W. S. Brown, D. F. Marshall, and M. Echeverria, “Intronic noncoding RNAs and splicing,” Trends in Plant Science, vol. 13, no. 7, pp. 335–342, 2008. View at Publisher · View at Google Scholar · View at Scopus
  162. J. Hirsch, V. Lefort, M. Vankersschaver et al., “Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts,” Plant Physiology, vol. 140, no. 4, pp. 1192–1204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  163. K. Yan, P. Liu, C.-A. Wu et al., “Stress-induced alternative splicing provides a mechanism for the regulation of MicroRNA processing in Arabidopsis thaliana,” Molecular Cell, vol. 48, no. 4, pp. 521–531, 2012. View at Publisher · View at Google Scholar · View at Scopus
  164. R. Schwab, C. Speth, S. Laubinger, and O. Voinnet, “Enhanced microRNA accumulation through stemloop-adjacent introns,” EMBO Reports, vol. 14, no. 7, pp. 615–621, 2013. View at Publisher · View at Google Scholar · View at Scopus
  165. D. Bielewicz, M. Kalak, M. Kalyna et al., “Introns of plant pri-miRNAs enhance miRNA biogenesis,” EMBO Reports, vol. 14, no. 7, pp. 622–628, 2013. View at Publisher · View at Google Scholar · View at Scopus
  166. T. Köster, K. Meyer, C. Weinholdt et al., “Regulation of pri-miRNA processing by the hnRNP-like protein AtGRP7 in Arabidopsis,” Nucleic Acids Research, vol. 42, no. 15, pp. 9925–9936, 2014. View at Publisher · View at Google Scholar
  167. S. Ben Chaabane, R. Liu, V. Chinnusamy et al., “STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis,” Nucleic Acids Research, vol. 41, no. 3, pp. 1984–1997, 2013. View at Publisher · View at Google Scholar · View at Scopus
  168. K. Baerenfaller, R. Bastow, J. Benyon et al., “Taking the next step: building an Arabidopsis information portal,” The Plant Cell, vol. 24, no. 6, pp. 2248–2256, 2012. View at Google Scholar
  169. A. S. N. Reddy, M. F. Rogers, D. N. Richardson, M. Hamilton, and A. Ben-Hur, “Deciphering the plant splicing code: experimental and computational approaches for predicting alternative splicing and splicing regulatory elements,” Frontiers in Plant Science, vol. 3, article 18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. X. Gan, O. Stegle, J. Behr et al., “Multiple reference genomes and transcriptomes for Arabidopsis thaliana,” Nature, vol. 477, no. 7365, pp. 419–423, 2011. View at Publisher · View at Google Scholar · View at Scopus
  171. M. J. Muñoz, M. de la Mata, and A. R. Kornblihtt, “The carboxy terminal domain of RNA polymerase II and alternative splicing,” Trends in Biochemical Sciences, vol. 35, no. 9, pp. 497–504, 2010. View at Publisher · View at Google Scholar · View at Scopus
  172. A. R. Kornblihtt, “Chromatin, transcript elongation and alternative splicing,” Nature Structural and Molecular Biology, vol. 13, no. 1, pp. 5–7, 2006. View at Publisher · View at Google Scholar · View at Scopus
  173. R. F. Luco, M. Allo, I. E. Schor, A. R. Kornblihtt, and T. Misteli, “Epigenetics in alternative pre-mRNA splicing,” Cell, vol. 144, no. 1, pp. 16–26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  174. R. F. Luco, Q. Pan, K. Tominaga, B. J. Blencowe, O. M. Pereira-Smith, and T. Misteli, “Regulation of alternative splicing by histone modifications,” Science, vol. 327, no. 5968, pp. 996–1000, 2010. View at Publisher · View at Google Scholar · View at Scopus
  175. R. Sen and S. D. Fugmann, “Transcription, splicing, and release: are we there yet?” Cell, vol. 150, no. 2, pp. 241–243, 2012. View at Publisher · View at Google Scholar · View at Scopus