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Regulation of RNA metabolism in plant development and stress responses

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Abstract

Posttranscriptional regulation of RNA metabolism, including RNA processing, splicing, editing, transport, translational control and turnover, is a key regulatory process in plant growth, development, and stress responses. A variety of RNA-binding proteins (RBPs) plays central roles during these cellular processes. Over the last decades, a considerable progress has been made in the identification and functional analysis of RBPs involved in growth, development, and stress response of plants. Identification of different family members of RBPs and determination of their functional roles in RNA metabolism shed light on the importance of the regulation of RNA metabolism and the role of RBPs as a central regulator in diverse cellular processes. In particular, recent reports demonstrate the emerging idea that certain RBPs perform a function as RNA chaperones during growth, development, and stress response of plants.

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References

  • Albà MM, Pagès M (1998) Plant proteins containing the RNA-recognition motif. Trends Plant Sci 3:15–21

    Article  Google Scholar 

  • Aneeta NS-M, Tuteja N, Sopory SK (2002) Salinity- and ABAinduced up-regulation and light-mediated modulation of mRNA encoding glycine-rich RNA-binding protein from Sorghum bicolor. Biochem Biophys Res Commun 296:1063–1068

    Article  PubMed  CAS  Google Scholar 

  • Arthur DC, Ghetu AF, Gubbins MJ, Edwards RA, Frost LS, Glover JN (2003) FinO is an RNA chaperone that facilitates senseantisense RNA interactions. EMBO J 22:6346–6355

    Article  PubMed  CAS  Google Scholar 

  • Bae W, Xia B, Inouye M et al (2000) Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc Natl Acad Sci USA 97:7784–7789

    Article  PubMed  CAS  Google Scholar 

  • Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621

    Article  PubMed  CAS  Google Scholar 

  • del Campo M (2009) Post-transcriptional control of chloroplast gene expression. Gene Regul Syst Biol 3:31–47

    Google Scholar 

  • Chaikam V, Karlson D (2008) Functional characterization of two cold shock domain proteins from Oryza sativa. Plant Cell Environ 31:995–1006

    Article  PubMed  CAS  Google Scholar 

  • Chaikam V, Karlson D (2010) Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins. Biochem Mol Biol Rep 43:1–8

    CAS  Google Scholar 

  • Chambers JR and Bender KS (2011) The RNA chaperone Hfq is important for growth and stress tolerance in Francisella novicida. PLoS One 6:e19797

    Article  PubMed  CAS  Google Scholar 

  • Chaulk SG, Smith Frieday MN, Arthur DC, Culham DE, Edwards RA, Soo P, Frost LS, Keates RA, Glover JN, Wood JM (2011) ProQ is an RNA chaperone that controls ProP levels in Escherichia coli. Biochemistry 50:3095–3106

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Zeng Q-C, Lu X-P, Yu D-Q, Li W-Z (2010) Characterization and expression analysis of four glycine-rich RNA-binding proteins involved in osmotic response in tobacco (Nicotiana tabacum cv. Xanthi). Agric Sci China 9:1577–1587

    Article  CAS  Google Scholar 

  • Cheng Y, Kato N, Wang W, Li J, Chen X (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4:53–66

    Article  PubMed  CAS  Google Scholar 

  • Chung E, Cho CW, Yun BH, Choi HK, So HA, Lee SW, Lee JH (2009) Molecular cloning and characterization of the soybean DEAD-box RNA helicase gene induced by low temperature and high salinity stress. Gene 443:91–99

    Article  PubMed  CAS  Google Scholar 

  • Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG (1993) HnRNP proteins and the biogenesis of mRNA. Ann Rev Biochem 62:289–321

    Article  PubMed  CAS  Google Scholar 

  • Ferullo JM, Vézina LP, Rail J, Laberge S, Nadeau P, Castonguay Y (1997) Differential accumulation of two glycine-rich proteins during cold-acclimation alfalfa. Plant Mol Biol 33:625–633

    Article  PubMed  CAS  Google Scholar 

  • Fusaro AF, Bocca SN, Ramos RLB, Rosa Maria Barroco RM, Magioli C, Jorge VC, Coutinho TC, Rangel-Lima CM, Rycke RD, Inze D, Engler G, Sachetto-Martins G (2011) AtGRP2, a cold-induced nucleo-cytoplasmic RNA-bindingprotein, has a role in flower and seed development. Plant Mol Biol Rep 29:761–768

    Article  Google Scholar 

  • Gómez J, Sánchez-Martínez D, Stiefel V et al (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 344:262–264

    Article  Google Scholar 

  • Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu JK (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci USA 99:11507–11512

    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 

  • Graumann PL, Marahiel MA (1998) A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23:286–290

    Article  PubMed  CAS  Google Scholar 

  • Guan Q, Wu J, Zhang Y, Jiang C, Liu R, Chai C, Zhu J (2013) A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25:342–56

    Article  PubMed  CAS  Google Scholar 

  • Herschlag D (1995) RNA chaperones and the RNA folding problem. J Biol Chem 270:20871–20874

    PubMed  CAS  Google Scholar 

  • Hirose T, Sugita M, Sugiura M (1994) Characterization of a cDNA encoding a novel type of RNA-binding protein in tobacco: its expression and nucleic acid-binding properties. Mol Gen Genet 244:360–366

    Article  PubMed  CAS  Google Scholar 

  • Huang HR, Rowe CE, Mohr S, Jiang Y, Lambowitz AM, Perlman PS (2005) The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc Natl Acad Sci USA 102:163–168

    Article  PubMed  CAS  Google Scholar 

  • Ivanyi-Nagy R, Davidovic L, Khandjian EW, Darlix JL (2005) Disordered RNA chaperone proteins: from functions to disease. Cell Mol Life Sci 62:1409–1417

    Article  PubMed  CAS  Google Scholar 

  • Ivanyi-Nagy R, Lavergne J-P, Gabus C, Ficheux D, Darlix J-L (2008) RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res 36:712–725

    Article  PubMed  CAS  Google Scholar 

  • Jankowsky E (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36:19–29

    Article  PubMed  CAS  Google Scholar 

  • Jiang W, Hon Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272:196–202

    Article  PubMed  CAS  Google Scholar 

  • Kang H, Park SJ, Kwak KJ (2013) Plant RNA chaperones in stress response. Trends Plant Sci 18:100–106

    Article  PubMed  CAS  Google Scholar 

  • Kant P, Kant S, Gordon M, Shaked R, Barak S (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol 145:814–830

    Article  PubMed  CAS  Google Scholar 

  • Karlson D, Nakaminami K, Toyomasu T, Imai R (2002) A coldregulated nucleic acid-binding protein of winter wheat shares a domain with bacterial cold shock proteins. J Biol Chem 277:35248–35256

    Article  PubMed  CAS  Google Scholar 

  • Karlson D, Imai R (2003) Conservation of the cold shock domain protein family in plants. Plant Physiol 131:12–15

    Article  PubMed  CAS  Google Scholar 

  • Kenan DJ, Query CC, Keene JD (1991) RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16:214–220

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Park SJ, Jang B, Jung C-H, Ahn SJ, Goh C-H, Cho K, Han O, Kang H (2007a) Functional characterization of a glycine-rich RNA-binding protein2 in Arabidopsis thaliana under abiotic stress conditions. Plant J 50:439–451

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH, Woo Y, Oh SH, Han YS, Kang H (2008a) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55:455–466

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Kim KA, Oh TR, Park CM, Kang H (2008b) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 49:1563–1571

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Park SJ, Kwak KJ, Kim YO, Kim JY, Song J, Jang B, Jung CH, Kang H (2007b) Cold shock domain proteins and glycinerich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res 35:506–516

    Article  PubMed  CAS  Google Scholar 

  • Kim M-H, Sasaki K, Imai R (2009) Cold shock domain protein 3 regulates freezing tolerance in Arabidopsis thaliana. J Biol Chem 284:23454–23460

    Article  PubMed  CAS  Google Scholar 

  • Kim YO, Kim JS, Kang H (2005) Cold-inducible zinc fingercontaining glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J 42:890–900

    Article  PubMed  CAS  Google Scholar 

  • Kim YO, Kang H (2006) The role of a zinc finger-containing glycinerich RNA-binding protein during the cold adaptation process in Arabidopsis thaliana. Plant Cell Physiol 47:793–798

    Article  PubMed  Google Scholar 

  • Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010a) Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J Exp Bot 61:2317–2325

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010b) Zinc finger-containing glycine-rich RNA-binding protein in Oryza sativa has an RNA chaperone activity under cold stress conditions. Plant Cell Environ 33:759–768

    Article  PubMed  CAS  Google Scholar 

  • Kim WY, Kim JY, Jung HJ, Oh SH, Han YS, Kang H (2010c) Comparative analysis of Arabidopsis zinc finger-containing glycine-rich RNA-binding proteins during cold adaptation. Plant Physiol Biochem 48:866–872

    Article  PubMed  CAS  Google Scholar 

  • Kim WY, Jung HJ, Kwak KJ, Kim MK, Oh SH, Han YS, Kang H (2010d) The Arabidopsis U12-types spliceosomal protein U11/U12-31K is involved in U12 intron splicing via RNA chaperone activity and affects plant development. Plant Cell 22:3951–3962

    Article  PubMed  CAS  Google Scholar 

  • Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J Exp Bot 56:3007–3016

    Article  PubMed  CAS  Google Scholar 

  • Kwak KJ, Jung HJ, Lee KH, Kim YS, Kim WY, Ahn SJ, Kang H (2012) The minor spliceosomal protein U11/U12-31K is an RNA chaperone crucial for U12 intron splicing and the development of dicot and monocot plants. PLoS ONE 7:e43707

    Article  PubMed  CAS  Google Scholar 

  • Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Kim J, Hong CB, Kim HJ, Park CM (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motif and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16:731–740

    Article  PubMed  CAS  Google Scholar 

  • Lohman TM (1992) Eschericia coli DNA helicases: mechanism of DNA unwinding. Mol Microbiol 6:5–14

    Article  PubMed  CAS  Google Scholar 

  • Lohman TM, Bjornson KP (1996) Mechanisms of helicase-catalyzed DNA unwinding. Ann Rev Biochem 65:169–214

    Article  PubMed  CAS  Google Scholar 

  • Lorkoviæ ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236

    Article  Google Scholar 

  • Lorkoviæ ZJ, Barta A (2002) Genomic 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

    Article  Google Scholar 

  • Lorsch JR (2002) RNA chaperones exist and DEAD-box proteins get a life. Cell 109:797–800

    Article  PubMed  CAS  Google Scholar 

  • Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domain. Cell 89:737–745

    Article  PubMed  CAS  Google Scholar 

  • Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5:99–104

    Article  PubMed  CAS  Google Scholar 

  • Martin SL (2010) Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1. RNA Biol 7:706–711

    Article  PubMed  CAS  Google Scholar 

  • Maruyama K, Sato N, Ohta N (1999) Conservation of structure and cold-regulation of RNA-binding proteis in cyanobacteria: probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acid Res 27:2029–2036

    Article  PubMed  CAS  Google Scholar 

  • Matson SW (1991) DNA helicases of Escherichia coli. Prog Nucleic Acid Res Mol Biol 40:2029–2036

    Google Scholar 

  • Matson SW, Bean D, George JW (1994) DNA helicases: enzymes with essential roles in all aspects of DNA metabolism. BioEssays 16:13–21

    Article  PubMed  CAS  Google Scholar 

  • Mockler TC, Yu X, Shalitin D, Parikh D, Michael TP, Liou J, Huang J, Smith Z, Alonso JM, Ecker JR, Chory J, Lin C (2004) Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci USA 101:12759–12764

    Article  PubMed  CAS  Google Scholar 

  • Mohr S, Stryker JM, Lambowitz AM (2002) DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109:769–779

    Article  PubMed  CAS  Google Scholar 

  • Mohr S., Matsuura M., Perlman PS, Lambowitz AM (2006) A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc Natl Acad Sci USA 103:3569–3574

    Article  PubMed  CAS  Google Scholar 

  • Nagai K, Oubridge C, Ito N, Avis J, Evans P (1995) The RNP domain: a sequence specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem Sci 20:235–240

    Article  PubMed  CAS  Google Scholar 

  • Nakaminami K, Karlson D, Imai R (2006) Functional conservation of cold shock domains in bacteria and higher plants. Proc Natl Acad Sci USA 103:10122–10127

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Muramoto Y, Takabe T (2004) Structural and transcriptional characterization of a salt-responsive gene encoding putative ATP-dependent RNA helicase in barley. Plant Sci 167:63–70

    Article  CAS  Google Scholar 

  • van Nocker S, Vierstra RD (1993) Two cDNAs from Arabidopsis thaliana encode putative RNA binding proteins containing glycinerich domains. Plant Mol Biol 21:695–699

    Article  PubMed  Google Scholar 

  • Nomata T, Kabeya Y, Sato N (2004) Cloning and characterization of glycine-rich RNA-binding protein cDNAs in the moss Physcomitrella patens. Plant Cell Physiol 45:48–56

    Article  PubMed  CAS  Google Scholar 

  • Park SJ, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010) The C-terminal zinc finger domain of Arabidopsis cold shock domain proteins is important for RNA chaperone activity during cold adaptation. Phytochem 71:543–547

    Article  CAS  Google Scholar 

  • Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133

    PubMed  CAS  Google Scholar 

  • Phadtare S, Inouye M, Severinov K (2002) The nucleic acid melting activity of Escherichia coli CspE is critical for transcription antitermination and cold acclimation of cells. J Biol Chem 277:7239–7245

    Article  PubMed  CAS  Google Scholar 

  • Rabhi M, Espéli O, Schwartz A, Cayrol B, Rahmouni AR, Arluison V, Boudvillain M (2011) The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J 30:2805–2816

    Article  PubMed  CAS  Google Scholar 

  • Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, Mayer O, Jantsch MF, Konrat R, Bläsi U, Schroeder R (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol 4:118–130

    Article  PubMed  CAS  Google Scholar 

  • Rajkowitsch L, Semrad K, Mayer O, Schroeder R (2005) Assays for the RNA chaperone activity of proteins. Biochem Soc Trans 33:450–456

    Article  PubMed  CAS  Google Scholar 

  • Ripoll JJ, Ferrándiz C, Martínez-Laborda A, Vera A (2006) PEPPER, a novel K-homology domain gene, regulates vegetative and gynoecium development in Arabidopsis. Dev Biol 289:346–359

    Article  PubMed  Google Scholar 

  • Russell AG, Charette JM, Spencer DF, Gray MW (2006) An early evolutionary origin for the minor spliceosome. Nature 443:863–866

    Article  PubMed  CAS  Google Scholar 

  • Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycinerich proteins: a family or just proteins with a common motif? Biochim Biophys Acta 1492:1–14

    Article  PubMed  CAS  Google Scholar 

  • Sasaki K, Imai R (2012) Pleiotropic roles of cold shock domain proteins in plants. Front Plant Sci 2:116

    Article  Google Scholar 

  • Sasaki K, Kim MH, Imai R (2007) Arabidopsis cold shock domain protein2 is a RNA chaperone that is regulated by cold and developmental signals. Biochem Biophys Res Commun 364:633–638

    Article  PubMed  CAS  Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670.

    Article  PubMed  CAS  Google Scholar 

  • Schroeder R, Barta A, Semrad K (2004) Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 5:908–919

    Article  PubMed  CAS  Google Scholar 

  • Semrad K (2011) Proteins with RNA chaperone activity: A world of diverse proteins with a common task-Impediment of RNA misfolding. Biochem Res Int ID 532908:1–11

    Article  Google Scholar 

  • Shinozuka H, Hisano H, Yoneyama S, Shimamoto Y, Jones ES, Forster JW, Yamada T, Kanazawa A (2006) Gene expression and genetic mapping analyses of a perennial ryegrass glycine-rich RNA-binding protein gene suggest a role in cold adaptation. Mol Genet Genom 275:399–408

    Article  CAS  Google Scholar 

  • Simpson GG, Filipowicz W (1996) Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organization of the spliceosomal machinery. Plant Mol Biol 32:1–41

    Article  PubMed  CAS  Google Scholar 

  • Stephen JR, Dent KC, Finch-Savage WE (2003) A cDNA encoding a cold-induced glycine-rich RNA binding protein from Prunus avium expressed in embryonic axes. Gene 320:177–183

    Article  PubMed  CAS  Google Scholar 

  • Stern DB, Goldschmidt-Clermont M & Hanson MR (2010) Chloroplast RNA metabolism. Ann Rev Plant Biol 61:125–155

    Article  CAS  Google Scholar 

  • Streitner C, Danisman S, Wehrle F, Schöning JC, Alfano JR, Staiger D (2008) The small glycine-rich RNA-binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. Plant J 56:239–250

    Article  PubMed  CAS  Google Scholar 

  • Tripurani SK, Nakaminami K, Thompson KB, Crowell SV, Guy CL, Karlson DT (2011) Spatial and temporal expression of coldresponsive DEAD-box RNA helicases reveals their functional roles during embryogenesis in Arabidopsis thaliana. Plant Mol Biol Rep 29:761–768

    Article  CAS  Google Scholar 

  • Tanner NK, Linder P (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8:251–262

    Article  PubMed  CAS  Google Scholar 

  • Tompa P, Kovacs D (2010) Intrinsically disordered chaperones in plants and animals. Biochem Cell Biol 88:167–174

    Article  PubMed  CAS  Google Scholar 

  • Tripurani SK, Nakaminami K, Thompson KB, Crowell SV, Guy CL, Karlson DT (2011) Spatial and temporal expression of coldresponsive DEAD-box RNA helicases reveals their functional roles during embryogenesis in Arabidopsis thaliana. Plant Mol Biol Rep 29:761–768

    Article  CAS  Google Scholar 

  • Tuteja N, Tuteja R (2004) Unraveling DNA helicases. Motif, structure, mechanism and function. Eur J Biochem 271:1849–1863

    Article  PubMed  CAS  Google Scholar 

  • Umate P, Tuteja R, Tuteja N (2010) Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human. Plant Mol Biol 73:449–465

    Article  PubMed  CAS  Google Scholar 

  • West SC (1996) DNA helicases: new breeds of translocating motors and molecular pumps. Cell 86:177–180

    Article  PubMed  CAS  Google Scholar 

  • Will CL, Schneider C, Hossbach M, Urlaub H, Rauhut R, Elbashir S, Tuschl T, Lührmann R (2004) The human 18S U11/U12 snRNP contains a set of novel proteins not found in the U2-dependent spliceosome. RNA 10:929–941

    Article  PubMed  CAS  Google Scholar 

  • Woodson SA (2010) Taming free energy landscapes with RNA chaperones. RNA Biol 7:677–686

    Article  PubMed  CAS  Google Scholar 

  • Xuan C, ZENG Qian-chun Z, Xiu-ping L, Di-qiu Y, Wen-zheng L (2010) Characterization and expression analysis of four glycinerich RNA-binding proteins involved in osmotic response in Tobacco (Nicotiana tabacum cv. Xanthi). Agri Sci China 9:1577–1587

    Article  Google Scholar 

  • Zhao X, Jain C (2011) DEAD-box proteins from Escherichia coli exhibit multiple ATP-independent activities. J Bacteriol 193:2236–2241

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Dong C-H, Zhu J-K (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295

    Article  PubMed  CAS  Google Scholar 

  • Zúñiga A, Hödar C, Hanna P, Ibáñez F, Moreno P, Pulgar R, Pastenes L, González M, Cambiazo V (2009) Genes encoding novel secreted and transmembrane proteins are temporally and spatially regulated during Drosophila melanogaster embryogenesis. BMC Biol 7:61

    Article  PubMed  Google Scholar 

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Jung, H.J., Park, S.J. & Kang, H. Regulation of RNA metabolism in plant development and stress responses. J. Plant Biol. 56, 123–129 (2013). https://doi.org/10.1007/s12374-013-0906-8

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