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RNA Regulation in Plant Cold Stress Response

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Survival Strategies in Extreme Cold and Desiccation

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1081))

Abstract

In addition to plants, all organisms react to environmental stimuli via the perception of signals and subsequently respond through alterations of gene expression. However, genes/mRNAs are usually not the functional unit themselves, and instead, resultant protein products with individual functions result in various acquired phenotypes. In order to fully characterize the adaptive responses of plants to environmental stimuli, it is essential to determine the level of proteins, in addition to the regulation of mRNA expression. This regulatory step, which is referred to as “mRNA posttranscriptional regulation,” occurs subsequent to mRNA transcription and prior to translation. Although these RNA regulatory mechanisms have been well-studied in many organisms, including plants, it is not fully understood how plants respond to environmental stimuli, such as cold stress, via these RNA regulations.

A recent study described several RNA regulatory factors in relation to environmental stress responses, including plant cold stress tolerance. In this chapter, the functions of RNA regulatory factors and comprehensive analyses related to the RNA regulations involved in cold stress response are summarized, such as mRNA maturation, including capping, splicing, polyadenylation of mRNA, and the quality control system of mRNA; mRNA degradation, including the decapping step; and mRNA stabilization. In addition, the putative roles of messenger ribonucleoprotein (mRNP) granules, such as processing bodies (PBs) and stress granules (SGs), which are cytoplasmic particles, are described in relation to RNA regulations under stress conditions. These RNA regulatory systems are important for adjusting or fine-tuning and determining the final levels of mRNAs and proteins in order to adapt or respond to environmental stresses. Collectively, these new areas of study revealed that plants possess precise novel regulatory mechanisms which specifically function in the response to cold stress.

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Abbreviations

CA:

Cold acclimation

CBF:

C-repeat-binding factors

DA:

Cold de-acclimation

DREB:

Dehydration-responsive element-binding proteins

hnRNPs:

Heterogeneous nuclear ribonucleoproteins

mRNP:

Messenger ribonucleoprotein

NMD:

Nonsense-mediated decay

PBs:

Processing bodies

PTC:

Premature termination codon

RBPs:

RNA-binding proteins

RRM:

RNA recognition motif

SGs:

Stress granules

snRNP:

Small nuclear ribonucleoprotein particle

SR:

Serine-/arginine-rich

References

  • Abbasi N, Park YI, Choi SB (2013) RNA deadenylation and decay in plants. J Plant Biol 56:198–207

    Article  CAS  Google Scholar 

  • Ambrosone A, Costa A, Leone A, Grillo S (2012) Beyond transcription: RNA-binding proteins as emerging regulators of plant response to environmental constraints. Plant Sci 182:12–18

    Article  CAS  PubMed  Google Scholar 

  • Anderson P, Kedersha N (2009) Stress granules. Curr Biol 19:R397–R398

    Article  CAS  PubMed  Google Scholar 

  • Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R (2005) A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11:717–727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arae T, Isai S, Sakai A, Mineta K, Yokota Hirai M, Suzuki Y, Kanaya S, Yamaguchi J, Naito S, Chiba Y (2017) Co-ordinated regulations of mRNA synthesis and decay during cold acclimation in Arabidopsis cells. Plant Cell Physiol 58:1090–1102

    Article  CAS  PubMed  Google Scholar 

  • Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Sorenson R, Juntawong P (2009) Getting the message across: cytoplasmic ribonucleoprotein complexes. Trends Plant Sci 14:443–453

    Article  CAS  PubMed  Google Scholar 

  • Barta A, Kalyna M, Reddy AS (2010) Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22:2926–2929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 12:96–102

    Article  CAS  PubMed  Google Scholar 

  • Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126:37–47

    Article  CAS  PubMed  Google Scholar 

  • Buchan JR, Muhlrad D, Parker R (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183:441–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang CT, Bercovich N, Loh B, Jonas S, Izaurralde E (2014) The activation of the decapping enzyme DCP2 by DCP1 occurs on the EDC4 scaffold and involves a conserved loop in DCP1. Nucleic Acids Res 42:5217–5233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chekanova JA, Shaw RJ, Wills MA, Belostotsky DA (2000) Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8S rRNA processing and mRNA decay defects of the yeast ski6 mutant and is found in an exosome-sized complex in plant and yeast cells. J Biol Chem 275:33158–33166

    Article  CAS  PubMed  Google Scholar 

  • Chen HC, Tseng CK, Tsai RT, Chung CS, Cheng SC (2013a) Link of NTR-mediated spliceosome disassembly with DEAH-box ATPases Prp2, Prp16, and Prp22. Mol Cell Biol 33:514–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen T, Cui P, Chen H, Ali S, Zhang S, Xiong L (2013b) A KH-domain RNA-binding protein interacts with FIERY2/CTD phosphatase-like 1 and splicing factors and is important for pre-mRNA splicing in Arabidopsis. PLoS Genet 9:e1003875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen T, Cui P, Xiong L (2015) The RNA-binding protein HOS5 and serine/arginine-rich proteins RS40 and RS41 participate in miRNA biogenesis in Arabidopsis. Nucleic Acids Res 43:8283–8298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiba Y, Green PJ (2009) mRNA degradation machinery in plants. J Plant Biol 52:114–124

    Article  CAS  Google Scholar 

  • Chiba Y, Mineta K, Hirai MY, Suzuki Y, Kanaya S, Takahashi H, Onouchi H, Yamaguchi J, Naito S (2013) Changes in mRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol 54:180–194

    Article  CAS  PubMed  Google Scholar 

  • Cordin O, Beggs JD (2013) RNA helicases in splicing. RNA Biol 10:83–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordin O, Hahn D, Beggs JD (2012) Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 24:431–438

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    Article  CAS  PubMed  Google Scholar 

  • Decker CJ, Parker R (2012) P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol 4:a012286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deshmukh MV, Jones BN, Quang-Dang DU, Flinders J, Floor SN, Kim C, Jemielity J, Kalek M, Darzynkiewicz E, Gross JD (2008) mRNA decapping is promoted by an RNA-binding channel in Dcp2. Mol Cell 29:324–336

    Article  CAS  PubMed  Google Scholar 

  • Dong MA, Farre EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci U S A 108:7241–7246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du JL, Zhang SW, Huang HW, Cai T, Li L, Chen S, He XJ (2015) The splicing factor PRP31 is involved in transcriptional gene silencing and stress response in Arabidopsis. Mol Plant 8:1053–1068

    Article  CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV, Zhuravlev YN (2013) The role of canonical and noncanonical pre-mRNA splicing in plant stress responses. Biomed Res Int 2013:264314

    Article  CAS  PubMed  Google Scholar 

  • Duque P (2011) A role for SR proteins in plant stress responses. Plant Signal Behav 6:49–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferraiuolo MA, Basak S, Dostie J, Murray EL, Schoenberg DR, Sonenberg N (2005) A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J Cell Biol 170:913–924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Floris M, Mahgoub H, Lanet E, Robaglia C, Menand B (2009) Post-transcriptional regulation of gene expression in plants during abiotic stress. Int J Mol Sci 10:3168–3185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fourmann JB, Tauchert MJ, Ficner R, Fabrizio P, Luhrmann R (2017) Regulation of Prp43-mediated disassembly of spliceosomes by its cofactors Ntr1 and Ntr2. Nucleic Acids Res 45:4068–4080

    Article  CAS  PubMed  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franks TM, Lykke-Andersen J (2008) The control of mRNA decapping and P-body formation. Mol Cell 32:605–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goeres DC, Van Norman JM, Zhang W, Fauver NA, Spencer ML, Sieburth LE (2007) Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell 19:1549–1564

    Article  CAS  PubMed  PubMed Central  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 25:342–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hausmann S, Koiwa H, Krishnamurthy S, Hampsey M, Shuman S (2005) Different strategies for carboxyl-terminal domain (CTD) recognition by serine 5-specific CTD phosphatases. J Biol Chem 280:37681–37688

    Article  CAS  PubMed  Google Scholar 

  • Hershey JW, Sonenberg N, Mathews MB (2012) Principles of translational control: an overview. Cold Spring Harb Perspect Biol 4:a011528

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hirayama T, Matsuura T, Ushiyama S, Narusaka M, Kurihara Y, Yasuda M, Ohtani M, Seki M, Demura T, Nakashita H et al (2013) A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis. Nat Commun 4:2247

    Article  PubMed  CAS  Google Scholar 

  • Hirsch J, Misson J, Crisp PA, David P, Bayle V, Estavillo GM, Javot H, Chiarenza S, Mallory AC, Maizel A et al (2011) A novel fry1 allele reveals the existence of a mutant phenotype unrelated to 5′->3′ exoribonuclease (XRN) activities in Arabidopsis thaliana roots. PLoS One 6:e16724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hogg R, Mcgrail JC, O’keefe RT (2010) The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Biochem Soc Trans 38:1110–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K (2004) Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res 32:5096–5103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inada T (2017) The ribosome as a platform for mRNA and nascent polypeptide quality control. Trends Biochem Sci 42:5–15

    Article  CAS  PubMed  Google Scholar 

  • James AB, Syed NH, Bordage S, Marshall J, Nimmo GA, Jenkins GI, Herzyk P, Brown JW, Nimmo HG (2012) Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24:961–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang J, Wang B, Shen Y, Wang H, Feng Q, Shi H (2013) The Arabidopsis RNA binding protein with K homology motifs, SHINY1, interacts with the C-terminal domain phosphatase-like 1 (CPL1) to repress stress-inducible gene expression. PLoS Genet 9:e1003625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 38:823–839

    Article  CAS  PubMed  Google Scholar 

  • Kervestin S, Jacobson A (2012) NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Biol 13:700–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim E, Magen A, Ast G (2007a) Different levels of alternative splicing among eukaryotes. Nucleic Acids Res 35:125–131

    Article  CAS  PubMed  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 glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res 35:506–516

    Article  CAS  PubMed  Google Scholar 

  • Kim GD, Cho YH, Lee BH, Yoo SD (2017) Stabilized1 modulates pre-mRNA splicing for thermotolerance. Plant Physiol 173:2370–2382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koiwa H, Hausmann S, Bang WY, Ueda A, Kondo N, Hiraguri A, Fukuhara T, Bahk JD, Yun DJ, Bressan RA et al (2004) Arabidopsis C-terminal domain phosphatase-like 1 and 2 are essential Ser-5-specific C-terminal domain phosphatases. Proc Natl Acad Sci U S A 101:14539–14544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koncz C, Dejong F, Villacorta N, Szakonyi D, Koncz Z (2012) The spliceosome-activating complex: molecular mechanisms underlying the function of a pleiotropic regulator. Front Plant Sci 3:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ (2013) Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 14:153–165

    Article  CAS  PubMed  Google Scholar 

  • Kumakura N, Otsuki H, Tsuzuki M, Takeda A, Watanabe Y (2013) Arabidopsis AtRRP44A is the functional homolog of Rrp44/Dis3, an exosome component, is essential for viability and is required for RNA processing and degradation. PLoS One 8:e79219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak KJ, Park SJ, Han JH, Kim MK, Oh SH, Han YS, Kang H (2011) Structural determinants crucial to the RNA chaperone activity of glycine-rich RNA-binding proteins 4 and 7 in Arabidopsis thaliana during the cold adaptation process. J Exp Bot 62:4003–4011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon YJ, Park MJ, Kim SG, Baldwin IT, Park CM (2014) Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant Biol 14:136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lazar G, Goodman HM (2000) The Arabidopsis splicing factor SR1 is regulated by alternative splicing. Plant Mol Biol 42:571–581

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Kang H (2016) Emerging roles of RNA-binding proteins in plant growth, development, and stress responses. Mol Cells 39:179–185

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei X, Xiao Y, Xia W, Mason AS, Yang Y, Ma Z, Peng M (2014) RNA-seq analysis of oil palm under cold stress reveals a different C-repeat binding factor (CBF) mediated gene expression pattern in Elaeis guineensis compared to other species. PLoS One 9:e114482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leviatan N, Alkan N, Leshkowitz D, Fluhr R (2013) Genome-wide survey of cold stress regulated alternative splicing in Arabidopsis thaliana with tiling microarray. PLoS One 8:e66511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Foster CM, Gan Q, Nettleton D, James MG, Myers AM, Wurtele ES (2009) Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J 58:485–498

    Article  CAS  PubMed  Google Scholar 

  • Liang W, Li C, Liu F, Jiang H, Li S, Sun J, Wu X, Li C (2009) The Arabidopsis homologs of CCR4-associated factor 1 show mRNA deadenylation activity and play a role in plant defence responses. Cell Res 19:307–316

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Chen X (2016) RNA quality control as a key to suppressing RNA silencing of endogenous genes in plants. Mol Plant 9:826–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM (2013) Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76:101–114

    CAS  PubMed  Google Scholar 

  • Lloyd JP, Davies B (2013) SMG1 is an ancient nonsense-mediated mRNA decay effector. Plant J 76:800–810

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22:1184–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    Article  CAS  PubMed  Google Scholar 

  • Mastrangelo AM, Marone D, Laido G, De Leonardis AM, De Vita P (2012) Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci 185–186:40–49

    Article  PubMed  CAS  Google Scholar 

  • Merret R, Descombin J, Juan YT, Favory JJ, Carpentier MC, Chaparro C, Charng YY, Deragon JM, Bousquet-Antonelli C (2013) XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep 5:1279–1293

    Article  CAS  PubMed  Google Scholar 

  • Meyer K, Koester T, Staiger D (2015) Pre-mRNA splicing in plants: in vivo functions of RNA-binding proteins implicated in the splicing process. Biomol Ther 5:1717–1740

    CAS  Google Scholar 

  • Miller JE, Reese JC (2012) Ccr4-Not complex: the control freak of eukaryotic cells. Crit Rev Biochem Mol Biol 47:315–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motomura K, Le QT, Hamada T, Kutsuna N, Mano S, Nishimura M, Watanabe Y (2015) Diffuse decapping enzyme DCP2 accumulates in DCP1 foci under heat stress in Arabidopsis thaliana. Plant Cell Physiol 56:107–115

    Article  CAS  PubMed  Google Scholar 

  • Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107

    Article  CAS  PubMed  Google Scholar 

  • Nagarajan VK, Jones CI, Newbury SF, Green PJ (2013) XRN 5′ – >3′ exoribonucleases: structure, mechanisms and functions. Biochim Biophys Acta 1829:590–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50:447–462

    Article  CAS  PubMed  Google Scholar 

  • Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T (2012) Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc Natl Acad Sci U S A 109:17123–17128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakaminami K, Matsui A, Shinozaki K, Seki M (2012) RNA regulation in plant abiotic stress responses. Biochim Biophys Acta 1819:149–153

    Article  CAS  PubMed  Google Scholar 

  • Nakaminami K, Matsui A, Nakagami H, Minami A, Nomura Y, Tanaka M, Morosawa T, Ishida J, Takahashi S, Uemura M et al (2014) Analysis of differential expression patterns of mRNA and protein during cold-acclimation and de-acclimation in Arabidopsis. Mol Cell Proteomics 13:3602–3611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen AH, Matsui A, Tanaka M, Mizunashi K, Nakaminami K, Hayashi M, Iida K, Toyoda T, Nguyen DV, Seki M (2015) Loss of Arabidopsis 5–3′ exoribonuclease AtXRN4 function enhances heat stress tolerance of plants subjected to severe heat stress. Plant Cell Physiol 56:1762–1772

    Article  CAS  PubMed  Google Scholar 

  • Nguyen CC, Nakaminami K, Matsui A, Kobayashi S, Kurihara Y, Toyooka K, Tanaka M, Seki M (2016) Oligouridylate binding protein 1b plays in integral role in plant heat stress tolerance. Front Plant Sci 7:853

    PubMed  PubMed Central  Google Scholar 

  • Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann O (2010) Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol Life Sci 67:677–700

    Article  CAS  PubMed  Google Scholar 

  • Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Nishimura N, Okamoto M, Narusaka M, Yasuda M, Nakashita H, Shinozaki K, Narusaka Y, Hirayama T (2009) ABA hypersensitive germination2-1 causes the activation of both abscisic acid and salicylic acid responses in Arabidopsis. Plant Cell Physiol 50:2112–2122

    Article  CAS  PubMed  Google Scholar 

  • Noren L, Kindgren P, Stachula P, Ruhl M, Eriksson ME, Hurry V, Strand A (2016) Circadian and plastid signaling pathways are integrated to ensure correct expression of the CBF and COR genes during photoperiodic growth. Plant Physiol 171:1392–1406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nyiko T, Kerenyi F, Szabadkai L, Benkovics AH, Major P, Sonkoly B, Merai Z, Barta E, Niemiec E, Kufel J et al (2013) Plant nonsense-mediated mRNA decay is controlled by different autoregulatory circuits and can be induced by an EJC-like complex. Nucleic Acids Res 41:6715–6728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palusa SG, Reddy AS (2015) Differential recruitment of splice variants from SR pre-mRNAs to polysomes during development and in response to stresses. Plant Cell Physiol 56:421–427

    Article  CAS  PubMed  Google Scholar 

  • Palusa SG, Ali GS, Reddy AS (2007) Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J 49:1091–1107

    Article  CAS  PubMed  Google Scholar 

  • Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646

    Article  CAS  PubMed  Google Scholar 

  • Peccarelli M, Kebaara BW (2014) Regulation of natural mRNAs by the nonsense-mediated mRNA decay pathway. Eukaryot Cell 13:1126–1135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perea-Resa C, Hernandez-Verdeja T, Lopez-Cobollo R, Del Mar Castellano M, Salinas J (2012) LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell 24:4930–4947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perea-Resa C, Carrasco-Lopez C, Catala R, Tureckova V, Novak O, Zhang W, Sieburth L, Jimenez-Gomez JM, Salinas J (2016) The LSM1-7 complex differentially regulates Arabidopsis tolerance to abiotic stress conditions by promoting selective mRNA decapping. Plant Cell 28:505–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Ortin JE, Alepuz PM, Moreno J (2007) Genomics and gene transcription kinetics in yeast. Trends Genet 23:250–257

    Article  CAS  PubMed  Google Scholar 

  • Pierrat OA, Mikitova V, Bush MS, Browning KS, Doonan JH (2007) Control of protein translation by phosphorylation of the mRNA 5′-cap-binding complex. Biochem Soc Trans 35:1634–1637

    Article  CAS  PubMed  Google Scholar 

  • Reddy AS, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riehs N, Akimcheva S, Puizina J, Bulankova P, Idol RA, Siroky J, Schleiffer A, Schweizer D, Shippen DE, Riha K (2008) Arabidopsis SMG7 protein is required for exit from meiosis. J Cell Sci 121:2208–2216

    Article  CAS  PubMed  Google Scholar 

  • Rymarquis LA, Souret FF, Green PJ (2011) Evidence that XRN4, an Arabidopsis homolog of exoribonuclease XRN1, preferentially impacts transcripts with certain sequences or in particular functional categories. RNA 17:501–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoning JC, Streitner C, Meyer IM, Gao Y, Staiger D (2008) Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res 36:6977–6987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Mas P (2015) STRESSing the role of the plant circadian clock. Trends Plant Sci 20:230–237

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Kim MJ, Ryu JY, Jeong EY, Park CM (2011) Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nat Commun 2:303

    Article  PubMed  CAS  Google Scholar 

  • Shaul O (2015) Unique aspects of plant nonsense-mediated mRNA decay. Trends Plant Sci 20:767–779

    Article  CAS  PubMed  Google Scholar 

  • Shi C, Baldwin IT, Wu J (2012) Arabidopsis plants having defects in nonsense-mediated mRNA decay factors UPF1, UPF2, and UPF3 show photoperiod-dependent phenotypes in development and stress responses. J Integr Plant Biol 54:99–114

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Ye T, Zhong B, Liu X, Chan Z (2014) Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L.) Pers.) by exogenous calcium. J Integr Plant Biol 56:1064–1079

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    Article  CAS  PubMed  Google Scholar 

  • Shoemaker CJ, Green R (2012) Translation drives mRNA quality control. Nat Struct Mol Biol 19:594–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shuman S (2015) RNA capping: progress and prospects. RNA 21:735–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CW, Valcarcel J (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 25:381–388

    Article  CAS  PubMed  Google Scholar 

  • Sorenson R, Bailey-Serres J (2014) Selective mRNA sequestration by oligouridylate-binding protein 1 contributes to translational control during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A 111:2373–2378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staiger D, Brown JW (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25:3640–3656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Streitner C, Koster T, Simpson CG, Shaw P, Danisman S, Brown JW, Staiger D (2012) An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana. Nucleic Acids Res 40:11240–11125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki Y, Arae T, Green PJ, Yamaguchi J, Chiba Y (2015) AtCCR4a and AtCCR4b are involved in determining the poly(A) length of granule-bound starch synthase 1 transcript and modulating sucrose and starch metabolism in Arabidopsis thaliana. Plant Cell Physiol 56:863–874

    Article  CAS  PubMed  Google Scholar 

  • Walley JW, Kelley DR, Nestorova G, Hirschberg DL, Dehesh K (2010) Arabidopsis deadenylases AtCAF1a and AtCAF1b play overlapping and distinct roles in mediating environmental stress responses. Plant Physiol 152:866–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang BB, Brendel V (2004) The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol 5:R102

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber C, Nover L, Fauth M (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56:517–530

    Article  CAS  PubMed  Google Scholar 

  • Weill L, Belloc E, Bava FA, Mendez R (2012) Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol 19:577–585

    Article  CAS  PubMed  Google Scholar 

  • Wiederhold K, Passmore LA (2010) Cytoplasmic deadenylation: regulation of mRNA fate. Biochem Soc Trans 38:1531–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Witten JT, Ule J (2011) Understanding splicing regulation through RNA splicing maps. Trends Genet 27:89–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Lee H, Huang R, Zhu JK (2004) A single amino acid substitution in the Arabidopsis FIERY1/HOS2 protein confers cold signaling specificity and lithium tolerance. Plant J 40:536–545

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Chua NH (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell 21:3270–3279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Chua NH (2011) Processing bodies and plant development. Curr Opin Plant Biol 14:88–93

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Chua NH (2012) Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO J 31:1975–1984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Yang JY, Niu QW, Chua NH (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18:3386–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan C, Hang J, Wan R, Huang M, Wong CC, Shi Y (2015) Structure of a yeast spliceosome at 3.6-angstrom resolution. Science 349:1182–1191

    Article  CAS  PubMed  Google Scholar 

  • Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch-related alpha-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol 138:837–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeap WC, Namasivayam P, Ho CL (2014) HnRNP-like proteins as post-transcriptional regulators. Plant Sci 227:90–100

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Guo H (2017) mRNA decay in plants: both quantity and quality matter. Curr Opin Plant Biol 35:138–144

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Addepalli B, Yun KY, Hunt AG, Xu R, Rao S, Li QQ, Falcone DL (2008) A polyadenylation factor subunit implicated in regulating oxidative signaling in Arabidopsis thaliana. PLoS One 3:e2410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang J, Mao Z, Chong K (2013) A global profiling of uncapped mRNAs under cold stress reveals specific decay patterns and endonucleolytic cleavages in Brachypodium distachyon. Genome Biol 14:R92

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol 171:2744–2759

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank Dr. Dale T. Karlson and Dr. Akihiro Matsui for critical reading of this manuscript. This work is supported by Grants-in-Aid for Scientific Research, Grant Numbers 25850247 and 17K07690 to K.N. and 16H01476 to M.S.; on Innovative Areas (Thermal Biology) from MEXT, 18H04705 to M.S.; Japan Science and Technology Agency (JST), Core Research for Evolutionary Science and Technology (CREST), JPMJCR13B4 to M.S.; and Grants from RIKEN to M.S.

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Authors and Affiliations

  1. Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan

    Kentaro Nakaminami & Motoaki Seki

  2. Plant Epigenome Regulation Laboratory, Cluster for Pioneering Research, RIKEN, Wako, Saitama, Japan

    Motoaki Seki

  3. Kihara Institute for Biological Research, Yokohama City University, Yokohama, Kanagawa, Japan

    Motoaki Seki

  4. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology (JST), Kawaguchi, Saitama, Japan

    Motoaki Seki

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  1. Kentaro Nakaminami
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Correspondence to Kentaro Nakaminami .

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  1. Faculty of Agriculture, Kyushu University, Fukuoka, Japan

    Mari Iwaya-Inoue

  2. Center for Biological Resources and Informatics, Tokyo Institute of Technology, Yokohama, Japan

    Minoru Sakurai

  3. United Graduate School of Agricultural Sciences and Department of Plant-biosciences, Faculty of Agriculture, Iwate University, Morioka, Japan

    Matsuo Uemura

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Nakaminami, K., Seki, M. (2018). RNA Regulation in Plant Cold Stress Response. In: Iwaya-Inoue, M., Sakurai, M., Uemura, M. (eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology, vol 1081. Springer, Singapore. https://doi.org/10.1007/978-981-13-1244-1_2

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