A homolog of splicing factor SF1 is essential for development and is involved in the alternative splicing of pre‐mRNA in Arabidopsis thaliana
Tóm tắt
Summary During initial spliceosome assembly, SF1 binds to intron branch points and interacts with U2 snRNP auxiliary factor 65 (U2AF65). Here, we present evidence indicating that AtSF1, the Arabidopsis SF1 homolog, interacts with AtU2AF65a and AtU2AF65b, the Arabidopsis U2AF65 homologs. A mutant allele of AtSF1 (At5g51300) that contains a T–DNA insertion conferred pleiotropic developmental defects, including early flowering and abnormal sensitivity to abscisic acid. An AtSF1 promoter‐driven GUS reporter assay showed that AtSF1 promoter activity was temporally and spatially altered, and that full AtSF1 promoter activity required a significant proportion of the coding region. DNA chip analyses showed that only a small proportion of the transcriptome was altered by more than twofold in either direction in the AtSF1 mutant. Expression of the mRNAs of many heat shock proteins was more than fourfold higher in the mutant strain; these mRNAs were among those whose expression was increased most in the mutant strain. An RT–PCR assay revealed an altered alternative splicing pattern for heat shock transcription factor HsfA2 (At2g26150) in the mutant; this altered splicing is probably responsible for the increased expression of the target genes induced by HsfA2. Altered alternative splicing patterns were also detected for the transcripts of other genes in the mutant strain. These results suggest that AtSF1 has functional similarities to its yeast and metazoan counterparts.
Từ khóa
#alternative splicing #SF1 #development #abnormal abscisic acid #Arabidopsis thaliana HeynhTài liệu tham khảo
Abovich, N. and Rosbash, M. (1997) Cross‐intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell, 89, 403–412.
Aki, S., Nakai, H., Aoyama, T., Oka, A. and Tsuge, T. (2011) AtSAP130/AtSF3b–3 function is required for reproduction in Arabidopsis thaliana. Plant Cell Physiol. 52, 1330–1339.
Aparicio, F., Thomas, C.L., Lederer, C., Niu, Y., Wang, D. and Maule, A.J. (2005) Virus induction of heat shock protein 70 reflects a general response to protein accumulation in the plant cytosol. Plant Physiol. 138, 529–536.
Arciga‐Reyes, L., Wootton, L., Kieffer, M. and Davies, B. (2006) UPF1 is required for nonsense‐mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 47, 480–489.
Arning, S., Grüter, P., Bilbe, G. and Krämer, A. (1996) Mammalian splicing factor SF1 is encoded by variant cDNAs and binds to RNA. RNA 2, 794–810.
Barbazuk, W.B., Fu, Y. and McGinnis, K.M. (2008) Genome‐wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res. 18, 1381–1392.
Berglund, J.A., Chua, K., Abovich, N., Reed, R. and Rosbash, M. (1997) The splicing factor BBP interacts specifically with the pre‐mRNA branchpoint sequence UACUAAC. Cell, 89, 781–787.
Bezerra, I.C., Michaels, S.D., Schomburg, F.M. and Amasino, R.M. (2004) Lesions in the mRNA cap‐binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA‐mediated delayed flowering in Arabidopsis. Plant J. 40, 112–119.
Bracha‐Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S. and Ohad, N. (2004) Detection of protein–protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40, 419–427.
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.
Chen, R., Silver, D.L. and de Bruijin, F.J. (1998) Nodule parenchyma‐specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3' untranslated region. Plant Cell, 10, 1585–1602.
Chung, T., Wang, D., Kim, C.S., Yadegari, R. and Larkins, B.A. (2009) Plant SMU–1 and SMU–2 homologues regulate pre‐mRNA splicing and multiple aspects of development. Plant Physiol. 151, 1498–1512.
Clark, T.A., Sugnet, C.W. and Ares, M. Jr (2002) Genome wide analysis of mRNA processing in yeast using splicing‐specific microarrays. Science, 296, 907–910.
Clarke, J.H., Tack, D., Findlay, K., Van Montagu, M. and Van Lijsebettens, M. (1999) The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J. 20, 493–501.
Corioni, M., Antih, N., Tanackovic, G., Zavolan, M. and Kramer, A. (2011) Analysis of in situ pre‐mRNA targets of human splicing factor SF1 reveals a function in alternative splicing. Nucleic Acids Res. 39, 1868–1879.
Fukumura, K., Kato, A., Jin, Y., Ideue, T., Hirose, T., Kataoka, N., Fujiwara, T., Sakamoto, H. and Inoue, K. (2007) Tissue‐specific splicing regulator Fox–1 induces exon skipping by interfering E complex formation on the downstream intron of human F1gamma gene. Nucleic Acids Res. 35, 5303–5311.
Galy, V., Gadal, O., Fromont‐Racine, M., Romano, A., Jacquier, A. and Nehrbass, U. (2004) Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell, 116, 63–73.
Garrey, S.M., Voelker, R. and Berglund, J.A. (2006) An extended RNA binding site for the yeast branch point‐binding protein and the role of its zinc knuckle domains in RNA binding. J. Biol. Chem. 281, 27443–27453.
Haraguchi, N., Andoh, T., Frendewey, D. and Tani, T. (2007) Mutations in the SF1–U2AF59–U2AF23 complex cause exon skipping in Schizosaccharomyces pombe. J. Biol. Chem. 282, 2221–2228.
Hori, K. and Watanabe, Y. (2005) UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J. 43, 530–540.
Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell, 136, 763–776.
Hugouvieux, V., Kwak, J.M. and Schroeder, J.I. (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell, 106, 477–487.
Jang, Y.H., Lee, J.H., Park, H.Y., Kim, S.K., Lee, B.Y., Suh, M.C. and Kim, J.K. (2009a) OsFCA transcripts show more complex alternative processing patterns than its Arabidopsis counterparts. J. Plant Biol. 52, 161–166.
Jang, Y.H., Park, H.Y., Kim, S.K., Lee, J.H., Suh, M.C., Chung, Y.S., Paek, K.H. and Kim, J.K. (2009b) Survey of rice proteins interacting with OsFCA and OsFY proteins which are homologous to the Arabidopsis flowering time proteins FCA and FY. Plant Cell Physiol. 50, 1479–1492.
Kielkopf, C.L., Lucke, S. and Green, M.R. (2004) U2AF homology motifs: protein recognition in the RRM world. Genes Dev. 18, 1513–1526.
Kim, W.Y., Jung, H.J., Kwak, K.J., Kim, M.K., Oh, S.H., Han, Y.S. and Kang, H. (2010) The Arabidopsis U12‐type spliceosomal protein U11/U12–31K is involved in U12 intron splicing via RNA chaperone activity and affects plant development. Plant Cell, 22, 3951–3962.
Kuhn, J.M., Boisson‐Dernier, A., Dizon, M.B., Maktabi, M.H. and Schroeder, J.I. (2006) The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 140, 127–139.
Kuhn, J.M., Breton, G. and Schroeder, J.I. (2007) mRNA metabolism of flowering‐time regulators in wild‐type Arabidopsis revealed by a nuclear cap binding protein mutant, abh1. Plant J. 50, 1049–1062.
Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y. and Nambara, E. (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'–hydroxylases: key enzymes in ABA catabolism. EMBO J. 23, 1647–1656.
Lee, J.H., Cho, Y.S., Yoon, H.S., Suh, M.C., Moon, J., Lee, I., Weigel, D., Yun, C.H. and Kim, J.K. (2005) Conservation and divergence of FCA function between Arabidopsis and rice. Plant Mol. Biol. 58, 823–838.
Lee, B.H., Kapoor, A., Zhu, J. and Zhu, J.K. (2006) STABILIZED1, a stress‐upregulated nuclear protein, is required for pre‐mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell, 18, 1736–1749.
Lin, K.T., Lu, R.M. and Tarn, W.Y. (2004) The WW domain‐containing proteins interact with the early spliceosome and participate in pre‐mRNA splicing in vivo. Mol. Cell. Biol. 24, 9176–9185.
Lorković, 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.
Lorković, Z.J., Wieczorek Kirk, D.A., Lambermon, M.H. and Filipowicz, W. (2000) Pre‐mRNA splicing in higher plants. Trends Plant Sci. 5, 160–167.
Mazroui, R., Puoti, A. and Krämer, A. (1999) Splicing factor SF1 from Drosophila and Caenorhabditis: presence of an N–terminal RS domain and requirement for viability. RNA, 5, 1615–1631.
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.
Moll, C., von Lyncker, L., Zimmermann, S., Kägi, C., Baumann, N., Twell, D., Grossniklaus, U. and Gross‐Hardt, R. (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56, 913–921.
Monaghan, J. and Li, X. (2010) The HEAT repeat protein ILITYHIA is required for plant immunity. Plant Cell Physiol. 51, 742–753.
Monaghan, J., Xu, F., Gao, M., Zhao, Q., Palma, K., Long, C., Chen, S., Zhang, Y. and Li, X. (2009) Two Prp19‐like U–box proteins in the MOS4‐associated complex play redundant roles in plant innate immunity. PLoS Pathog. 5, e1000526.
Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. and Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535–547.
Ohtani, M., Demura, T. and Sugiyama, M. (2013) Arabidopsis ROOT INITIATION DEFECTIVE1, a DEAH‐box RNA helicase involved in pre‐mRNA splicing, is essential for plant development. Plant Cell, 6, 2056–2069.
Park, J.W., Parisky, K., Celotto, A.M., Reenan, R.A. and Graveley, B.R. (2004) Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl Acad. Sci. USA, 101, 15974–15979.
Perea‐Resa, C., Hernández‐Verdeja, T., López‐Cobollo, R., del Mar Castellano, M. and Salinas, J. (2012) LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell 24, 4930–4947.
Pleiss, J.A., Whitworth, G.B., Bergkessel, M. and Guthrie, C. (2007) Transcript specificity in yeast pre‐mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol. 5, e90.
Prigge, M.J. and Wagner, D.R. (2001) The Arabidopsis SERRATE gene encodes a zinc‐finger protein required for normal shoot development. Plant Cell, 13, 1263–1279.
Rain, J.C., Rafi, Z., Rhani, Z., Legrain, P. and Kramer, A. (1998) Conservation of functional domains involved in RNA binding and protein–protein interactions in human and Saccharomyces cerevisiae pre‐mRNA splicing factor SF1. RNA, 4, 551–565.
Reddy, A.S. (2007) Alternative splicing of pre‐messenger RNAs in plants in the genomic era. Annu. Rev. Plant Biol. 58, 267–294.
Ru, Y., Wang, B.B. and Brendel, V. (2008) Spliceosomal proteins in plants. Curr. Top. Microbiol. Immunol. 326, 1–15.
Rutz, B. and Seraphin, B. (1999) Transient interaction of BBP/ScSF1 and Mud2 with the splicing machinery affects the kinetics of spliceosome assembly. RNA, 5, 819–831.
Rutz, B. and Séraphin, B. (2000) A dual role for BBP/ScSF1 in nuclear pre‐mRNA retention and splicing. EMBO J. 19, 1873–1886.
Sapra, A.K., Arava, Y., Khandelia, P. and Vijayraghavan, U. (2004) Genome‐wide analysis of pre‐mRNA splicing: intron features govern the requirement for the second step factor, Prp17 in Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Biol. Chem. 279, 52437–52446.
Schwartz, S.H., Silva, J., Burstein, D., Pupko, T., Eyras, E. and Ast, G. (2008) Large‐scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res. 18, 88–103.
Shitashige, M., Satow, R., Honda, K., Ono, M., Hirohashi, S. and Yamada, T. (2007) Increased susceptibility of Sf1+/− mice to azoxymethane‐induced colon tumorigenesis. Cancer Sci. 98, 1862–1867.
Sugio, A., Dreos, R., Aparicio, F. and Maule, A.J. (2009) The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell, 21, 642–654.
Sugliani, M., Brambilla, V., Clerkx, E.J., Koornneef, M. and Soppe, W.J. (2010) The conserved splicing factor SUA controls alternative splicing of the developmental regulator ABI3 in Arabidopsis. Plant Cell, 22, 1936–1946.
Tanackovic, G. and Krämer, A. (2005) Human splicing factor SF3a, but not SF1, is essential for pre‐mRNA splicing in vivo. Mol. Biol. Cell, 16, 1366–1377.
Thickman, K.R., Swenson, M.C., Kabogo, J.M., Gryczynski, Z. and Kielkopf, C.L. (2006) Multiple U2AF65 binding sites within SF3b155: thermodynamic and spectroscopic characterization of protein–protein interactions among pre‐mRNA splicing factors. J. Mol. Biol. 356, 664–683.
Voellmy, R. and Boellmann, F. (2007) Chaperone regulation of the heat shock protein response. Adv. Exp. Med. Biol. 594, 89–99.
Wahl, M.C., Will, C.L. and Lührmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701–718.
Wang, B.B. and Brendel, V. (2004) The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre‐mRNA splicing. Genome Biol. 5, R102.
Wang, B.B. and Brendel, V. (2006) Genome wide comparative analysis of alternative splicing in plants. Proc. Natl Acad. Sci. USA, 103, 7175–7180.
Wang, Q., Zhang, L., Lynn, B. and Rymond, B.C. (2008) A BBP–Mud2p heterodimer mediates branchpoint recognition and influences splicing substrate abundance in budding yeast. Nucleic Acids Res. 36, 2787–2798.
Will, C.L., Schneider, C., MacMillan, A.M., Katopodis, N.F., Neubauer, G., Wilm, M., Lührmann, R. and Query, C.C. (2001) A novel U2 and U11/U12 snRNP protein that associates with the pre‐mRNA branch site. EMBO J. 20, 4536–4546.
Worden, A.Z., Lee, J.H., Mock, T., Rouzé, P. and Simmons, M.P. (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science, 324, 268–272.
Xiong, L., Gong, Z., Rock, C.D., Subramanian, S., Guo, Y., Xu, W., Galbraith, D. and Zhu, J.K. (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm‐like protein in Arabidopsis. Dev. Cell, 1, 771–781.
Yagi, N., Takeda, S., Matsumoto, N. and Okada, K. (2009) VAJ/GFA1/CLO is involved in the directional control of floral organ growth. Plant Cell Physiol. 50, 515–527.
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, Z., Zhang, S., Zhang, Y. et al. (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre‐mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell, 23, 396–411.
Zhang, C.J., Zhou, J.X., Liu, J. et al. (2013) The splicing machinery promotes RNA‐directed DNA methylation and transcriptional silencing in Arabidopsis. EMBO J. 32, 1128–1140.