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mRNA Cap Binding Proteins: Effects on Abscisic Acid Signal Transduction, mRNA Processing, and Microarray Analyses

  • Chapter
Nuclear pre-mRNA Processing in Plants

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 326))

Abstract The plant hormone abscisic acid (ABA) intricately regulates a multitude of processes during plant growth and development. Recent studies have established a connection between genes participating in various steps of cellular RNA metabolism and the ABA signal transduction machinery. In this chapter we focus on the plant nuclear mRNA cap binding proteins, CBP20 and CBP80. We summarize and report recent findings on their effects on cellular signal transduction networks and mRNA processing events. ABA hypersensitive 1 (abh1) harbors a gene disruption in the Arabidopsis CBP80 gene. Loss-of-function mutation of ABH1 can also result in an early flowering phenotype in the Arabidopsis accession C24. abh1 revealed noncoding cis-natural antisense transcripts (cis-NATs) at the CONSTANS locus in wild-type plants with elevated cis-NAT expression in the mutant, abh1 also revealed an influence on the splicing of the MADS box transcription factor Flowering Locus C pre-mRNA, which may result in the regulation of flowering time. Furthermore, new experiments analyzing complementation of cpb20 with site-directed cpb20 mutants provide evidence that the CAP binding activity of CBP20 is essential for the observed cbp-associated phenotypes.

In conclusion, mutants in genes participating in RNA processing provide excellent tools to uncover novel molecular mechanisms for the regulation of RNA metabolism and of signal transduction networks in wild-type plants.

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References

  • Balatsos NAA, Nilsson P, Mazza C, Cusack S, Virtanen A (2006) Inhibition of mRNA deadenylation by the nuclear cap binding complex (CBC). J Biol Chem 281:4517–4522

    Article  PubMed  CAS  Google Scholar 

  • Bezerra IC, Michaels SD, Schomburg FM, Amasino RM (2004) Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. Plant J 40:112–119

    Article  PubMed  CAS  Google Scholar 

  • Calero G, Wilson KF, Ly T, Rios-Steiner JL, Clardy JC, Cerione RA (2002) Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol 9:912–917

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R (2006) Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127:1389–1400

    Article  PubMed  CAS  Google Scholar 

  • Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol (Stuttg) 8:314–325

    Article  CAS  Google Scholar 

  • Clark, TA, Sugnet, CW, Ares, M. Jr. (2002) Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296:907–910

    Article  PubMed  CAS  Google Scholar 

  • Faghihi M, Wahlestedt C (2006) RNA interference is not involved in natural antisense mediated regulation of gene expression in mammals. Genome Biol 7:R38

    Article  PubMed  Google Scholar 

  • Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546

    Article  PubMed  CAS  Google Scholar 

  • Fedoroff NV (2002) Cross-talk in abscisic acid signaling. Sci STKE 2002:RE10

    Article  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    PubMed  CAS  Google Scholar 

  • Flaherty SM, Fortes P, Izaurralde E, Mattaj IW, Gilmartin GM (1997) Participation of the nuclear cap binding complex in pre-mRNA 3′ processing. Proc Natl Acad Sci USA 94:11893–11898

    Article  PubMed  CAS  Google Scholar 

  • Fortes P, Inada T, Preiss T, Hentze MW, Mattaj IW, Sachs AB (2000) The yeast nuclear cap binding complex can interact with translation factor eIF4G and mediate translation initiation. Mol Cell 6:191–196

    Article  PubMed  CAS  Google Scholar 

  • Gao Q, Das B, Sherman F, Maquat LE (2005) Cap-binding protein 1-mediated and eukaryotic translation initiation factor 4E-mediated pioneer rounds of translation in yeast. Proc Natl Acad Sci USA 102:4258–4263

    Article  PubMed  CAS  Google Scholar 

  • Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD Box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267

    Article  PubMed  CAS  Google Scholar 

  • Gorlich D, Kraft R, Kostka S, Vogel F, Hartmann E, Laskey RA, Mattaj IW, Izaurraide E (1996) Importin provides a link between nuclear protein import and U snRNA export. Cell 87:21–32

    Article  PubMed  CAS  Google Scholar 

  • Guan LM, Zhao J, Scandalios JG (2000) Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  PubMed  CAS  Google Scholar 

  • Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093–1098

    Article  PubMed  CAS  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  PubMed  CAS  Google Scholar 

  • Hosoda N, Kim YK, Lejeune F, Maquat LE (2005) CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 12:893–901

    Article  PubMed  CAS  Google Scholar 

  • Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487

    Article  PubMed  CAS  Google Scholar 

  • Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI (2002) Localization, ion channel regulation, and genetic interactions during abscisic acid signaling of the nuclear mRNA cap-binding protein, ABH1. Plant Physiol 130:1276–1287

    Article  PubMed  CAS  Google Scholar 

  • Ishigaki Y, Li X, Serin G, Maquat LE (2001) Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607–617

    Article  PubMed  CAS  Google Scholar 

  • Israelsson M, Siegel RS, Young J, Hashimoto M, Iba K, Schroeder JI (2006) Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9:654–663

    Article  PubMed  CAS  Google Scholar 

  • Izaurralde E, Lewis J, McGuigan C, Jankowska M, Darzynkiewicz E, Mattaj IW (1994) A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78:657–668

    Article  PubMed  CAS  Google Scholar 

  • Johnson JM et al. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302:2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Kmieciak M, Simpson CG, Lewandowska D, Brown JWS, Jarmolowski A (2002) Cloning and characterization of two subunits of Arabidopsis thaliana nuclear cap-binding complex. Gene 283:171–183

    PubMed  CAS  Google Scholar 

  • Koornneef M, Leon-Kloosterziel KM, Schwartz SH, Zeevaart JAD (1998) The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiol Biochem 36:83–89

    Article  CAS  Google Scholar 

  • Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI (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

    Article  PubMed  CAS  Google Scholar 

  • Kuhn JM, Breton G, Schroeder JI (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

    Article  PubMed  CAS  Google Scholar 

  • Kuhn JM, Schroeder JI (2003) Impacts of altered RNA metabolism on abscisic acid signaling. Curr Opin Plant Biol 6:463–469

    Article  PubMed  CAS  Google Scholar 

  • Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Kapoor A, Zhu J, Zhu JK (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

    Article  PubMed  CAS  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448–1452

    Article  PubMed  CAS  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49:199–222

    Article  CAS  Google Scholar 

  • Lewis JD, Gorlich D, Mattaj IW (1996a) A yeast cap binding protein complex (yCBC) acts at an early step in pre-mRNA splicing. Nucl Acids Res 24:3332–3336

    Article  PubMed  CAS  Google Scholar 

  • Lewis JD, Izaurralde E (1997) The role of the cap structure in RNA processing and nuclear export. Eur J Biochem 247:461–469

    Article  PubMed  CAS  Google Scholar 

  • Lewis JD, Izaurralde E, Jarmolowski A, McGuigan C, Mattaj IW (1996b) A nuclear cap-binding complex facilitates association of U1 snRNP with the cap-proximal 5′ splice site. Genes Dev 10:1683–1698

    Article  PubMed  CAS  Google Scholar 

  • Li J, Kinoshita T, Pandey S, Ng CK, Gygi SP, Shimazaki K, Assmann SM (2002) Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 418:793–797

    Article  PubMed  CAS  Google Scholar 

  • Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300–303

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366

    Article  PubMed  CAS  Google Scholar 

  • MacRobbie EA (1998) Signal transduction and ion channels in guard cells. Philos Trans R Soc Lond B Biol Sci 353:1475–1488

    Article  PubMed  CAS  Google Scholar 

  • Makalowska I, Lin CF, Makalowski W (2005) Overlapping genes in vertebrate genomes. Comput Biol Chem 29:1–12

    Article  PubMed  CAS  Google Scholar 

  • Makarov EM, Makarova OV, Urlaub H, Gentzel M, Will CL, Wilm M, Luhrmann R (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298:2205–2208

    Article  PubMed  CAS  Google Scholar 

  • Maquat LE (2004) Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5:89–99

    Article  PubMed  CAS  Google Scholar 

  • Mazza C, Ohno M, Segref A, Mattaj IW, Cusack S (2001) Crystal structure of the human nuclear cap binding complex. Mol Cell 8:383–396

    Article  PubMed  CAS  Google Scholar 

  • Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264:1452–1455

    Article  PubMed  CAS  Google Scholar 

  • Mori IC et al. (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327

    Article  PubMed  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P) H and is differently disrupted upstream and downstream of reactive oxygen species production of abi1–1 and abi2–1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    Article  PubMed  CAS  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  PubMed  CAS  Google Scholar 

  • Nishimura N, Kitahata N, Seki M, Narusaka Y, Narusaka M, Kuromori T, Asami T, Shinozaki K, Hirayama T (2005) Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984

    Article  PubMed  CAS  Google Scholar 

  • Papp I, Mur LA, Dalmadi A, Dulai S, Koncz C (2004) A mutation in the Cap Binding Protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol Biol 55:679–686

    Article  PubMed  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  PubMed  CAS  Google Scholar 

  • Riera M, Redko Y, Leung J (2006) Arabidopsis RNA-binding protein UBA2a relocalizes into nuclear speckles in response to abscisic acid. FEBS Lett 580:4160–4165

    Article  PubMed  CAS  Google Scholar 

  • Schmidt C, Schelle I, Liao YJ, Schroeder JI (1995) Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. Proc Natl Acad Sci USA 92:9535–9539

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658

    Article  PubMed  CAS  Google Scholar 

  • Sheen J (1998) Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc Natl Acad Sci USA 95:975–980

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Katagiri T, Yamaguchi-Shinozaki K, Shinozaki K (2000) An Arabidopsis gene encoding a Ca2+-binding protein is induced by abscisic acid during dehydration. Plant Cell Physiol 41:898–903

    Article  PubMed  CAS  Google Scholar 

  • Uemura H, Jigami Y (1992) GCR3 encodes an acidic protein that is required for expression of glycolytic genes in Saccharomyces cerevisiae. J Bacteriol 174:5526–5532

    PubMed  CAS  Google Scholar 

  • Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351

    PubMed  CAS  Google Scholar 

  • Verslues PE, Zhu JK (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Guo Y, Dong CH, Ma W, Zhu JK (2006) Mutation of SAD2, an importin beta-domain protein in Arabidopsis, alters abscisic acid sensitivity. Plant J 47:776–787

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Chua NH, Wang XJ (2006) Prediction of trans-antisense transcripts in Arabidopsis thaliana. Genome Biol 7:R92

    Article  PubMed  Google Scholar 

  • Wang XJ, Gaasterland T, Chua NH (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6:R30

    Article  PubMed  Google Scholar 

  • Wilson KF, Cerione RA (2000) Signal transduction and post-transcriptional gene expression. Biol Chem 381:357–365

    Article  PubMed  CAS  Google Scholar 

  • Wilson KF, Fortes P, Singh US, Ohno M, Mattaj IW, Cerione RA (1999) The nuclear cap-binding complex is a novel target of growth factor receptor-coupled signal transduction. J Biol Chem 274:4166–4173

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Ruas P, Shen QJ (2005) Regulatory networks of the phytohormone abscisic acid. Vitam Horm 72:235–269

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1:771–781

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Licklider LJ, Gygi SP, Reed R (2002) Comprehensive proteomic analysis of the human spliceosome. Nature 419:182–185

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0116, USA

    J. M. Kuhn, V. Hugouvieux & J. I. Schroeder

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  1. J. M. Kuhn
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  2. V. Hugouvieux
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  3. J. I. Schroeder
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Editors and Affiliations

  1. Department of Biology and Program in Molecular Plant Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Anireddy S. N. Reddy

  2. Department of Microbiology, Thomas Jefferson University, Philadelphia, PA, 19107, USA

    Maxim Golovkin

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Kuhn, J.M., Hugouvieux, V., Schroeder, J.I. (2008). mRNA Cap Binding Proteins: Effects on Abscisic Acid Signal Transduction, mRNA Processing, and Microarray Analyses. In: Reddy, A.S.N., Golovkin, M. (eds) Nuclear pre-mRNA Processing in Plants. Current Topics in Microbiology and Immunology, vol 326. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-76776-3_8

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