Skip to main content
SpringerLink
Log in

RNA deadenylation and decay in plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

In eukaryotic cells, RNA levels are tightly regulated in a spatio-temporal manner to maintain the protein levels necessary for cell growth, differentiation and division. To cope with developmental and rapid environmental changes, RNAs that are no longer required by the cell undergo degradation via the mRNA decay process. A number of players involved in RNA degradation pathways have been identified for the last two decades. A wealth of information about the process of mRNA deadenylation and decay in yeast and other model organisms is currently available; however, very limited information is available in plants, including Arabidopsis. Nevertheless, the efforts of various plant research groups are continuously extending our understanding of this complicated process. Here, we summarize our current knowledge of RNA decay in yeast and compare this information with the progress from Arabidopsis. This review will especially focus on the structure and function of the deadenylation complex, 5′ to 3′ exoribonuclease (XRN)-mediated decay pathways and the exosome-mediated 3′ to 5′ decay pathway in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbasi N, Kim HB, Park N-i, Kim Y-K, Park Y-I, Choi S-B (2010) APUM23, a nucleolar Puf domain protein, is involved in preribosomal RNA processing and normal growth patterning in Arabidopsis. Plant J 64:960–976

    Article  PubMed  CAS  Google Scholar 

  • Abbasi N, Park Y-I, Choi S-B (2011) Pumilio Puf domain RNA-binding proteins in Arabidopsis. Plant Signal Behav 6: 364–368

    Article  PubMed  CAS  Google Scholar 

  • Allmang C, Petfalski E, Podtelejnikov A, Mann M, Tollervey D, Mitchell P (1999) The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes Dev 13:2148–2158

    Article  PubMed  CAS  Google Scholar 

  • Azzouz N, Panasenko OO, Colau G, Collart MA (2009) The CCR4-NOT complex physically and functionally interacts with TRAMP and the nuclear exosome. PLoS One 4:e6760

    Article  PubMed  Google Scholar 

  • Azzouz N, Panasenko OO, Deluen C, Hsieh J, Theiler G, Collart MA (2009) Specific roles for the Ccr4-Not complex subunits in expression of the genome. RNA 15:377–383

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chekanova JA, Dutko JA, Mian IS, Belostotsky DA (2002) Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′→5′ exonuclease containing S1 and KH RNA-binding domains. Nucleic Acids Res 30: 695–700

    Article  PubMed  CAS  Google Scholar 

  • Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R, Hooker T, Yazaki J, Li P, Skiba N, Peng Q, Alonso J, Brukhin V, Grossniklaus U, Ecker JR, Belostotsky DA (2007) Genomewide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340–1353

    Article  PubMed  CAS  Google Scholar 

  • Chekanova JA, Shaw RJ, Wills MA, Belostotsky DA (2000) Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8 S 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  PubMed  CAS  Google Scholar 

  • Chiba Y, Johnson MA, Lidder P, Vogel JT, van Erp H, Green PJ (2004) AtPARN is an essential poly(A) ribonuclease in Arabidopsis. Gene 328:95–102

    Article  PubMed  CAS  Google Scholar 

  • Chritton JJ, Wickens M (2010) Translational repression by PUF proteins in vitro. RNA 16:1217–1225

    Article  PubMed  CAS  Google Scholar 

  • Copeland PR, Wormington M (2001) The mechanism and regulation of deadenylation: identification and characterization of Xenopus PARN. RNA 7:875–886

    Article  PubMed  CAS  Google Scholar 

  • Cui Y, Ramnarain DB, Chiang YC, Ding LH, McMahon JS, Denis CL (2008) Genome wide expression analysis of the CCR4-NOT complex indicates that it consists of three modules with the NOT module controlling SAGA-responsive genes. Mol Genet Genomics 279:323–337

    Article  PubMed  CAS  Google Scholar 

  • Dehlin E, Wormington M, Korner CG, Wahle E (2000) Capdependent deadenylation of mRNA. EMBO J 19:1079–1086

    Article  PubMed  CAS  Google Scholar 

  • Dziembowski A, Lorentzen E, Conti E, Seraphin B (2007) A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14:15–22

    Article  PubMed  CAS  Google Scholar 

  • Egecioglu DE, Henras AK, Chanfreau GF (2006) Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12:26–32

    Article  PubMed  CAS  Google Scholar 

  • Garneau NL, Wilusz J, Wilusz CJ (2007) The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8:113–126

    Article  PubMed  CAS  Google Scholar 

  • Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–1048

    Article  PubMed  CAS  Google Scholar 

  • Gerber AP, Herschlag D, Brown PO (2004) Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2:E79

    Article  PubMed  Google Scholar 

  • Goldstrohm AC, Hook BA, Seay DJ, Wickens M (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13:533–539

    Article  PubMed  CAS  Google Scholar 

  • Goldstrohm AC, Seay DJ, Hook BA, Wickens M (2007) PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 282:109–114

    Article  PubMed  CAS  Google Scholar 

  • Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461

    Article  PubMed  CAS  Google Scholar 

  • Hooker TS, Lam P, Zheng H, Kunst L (2007) A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19:904–913

    Article  PubMed  CAS  Google Scholar 

  • Houseley J, LaCava J, Tollervey D (2006) RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7:529–539

    Article  PubMed  CAS  Google Scholar 

  • Houseley J, Tollervey D (2006) Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep 7:205–211

    Article  PubMed  CAS  Google Scholar 

  • Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136:763–776

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Takahashi A, Morita M, Suzuki T, Yamamoto T (2011) The role of the CNOT1 subunit of the CCR4-NOT complex in mRNA deadenylation and cell viability. Protein Cell 2:755–763

    Article  PubMed  CAS  Google Scholar 

  • Jia H, Wang X, Anderson JT, Jankowsky E (2012) RNA unwinding by the Trf4/Air2/Mtr4 polyadenylation (TRAMP) complex. Proc Natl Acad Sci USA 109:7292–7297

    Article  PubMed  CAS  Google Scholar 

  • Kastenmayer JP, Green PJ (2000) Novel features of the XRN-family in Arabidopsis: evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm. Proc Natl Acad Sci USA 97:13985–13990

    Article  PubMed  CAS  Google Scholar 

  • Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21:3123–3134

    Article  PubMed  CAS  Google Scholar 

  • Kerr SC, Azzouz N, Fuchs SM, Collart MA, Strahl BD, Corbett AH, Laribee RN (2011) The Ccr4-Not complex interacts with the mRNA export machinery. PLoS One 6:e18302

    Article  PubMed  CAS  Google Scholar 

  • LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713–724

    Article  PubMed  CAS  Google Scholar 

  • Lai WS, Kennington EA, Blackshear PJ (2003) Tristetraprolin and its family members can promote the cell-free deadenylation of AUrich element-containing mRNAs by poly(A) ribonuclease. Mol Cell Biol 23:3798–3812

    Article  PubMed  CAS  Google Scholar 

  • Lam P, Zhao L, McFarlane HE, Aiga M, Lam V, Hooker TS, Kunst L (2012) RDR1 and SGS3, components of RNA-mediated gene silencing, are required for the regulation of cuticular wax biosynthesis in developing inflorescence stems of Arabidopsis. Plant Physiol 159:1385–1395

    Article  PubMed  CAS  Google Scholar 

  • Lange H, Holec S, Cognat V, Pieuchot L, Le Ret M, Canaday J, Gagliardi D (2008) Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol Cell Biol 28:3038–3044

    Article  PubMed  CAS  Google Scholar 

  • Lange H, Sement FM, Gagliardi D (2011) MTR4, a putative RNA helicase and exosome co-factor, is required for proper rRNA biogenesis and development in Arabidopsis thaliana. Plant J 68: 51–63

    Article  PubMed  CAS  Google Scholar 

  • Lebreton A, Seraphin B (2008) Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim Biophys Acta 1779:558–565

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Liu Q, Greimann JC, Lima CD (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127:1223–1237

    Article  PubMed  CAS  Google Scholar 

  • Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495:70–75

    Article  PubMed  CAS  Google Scholar 

  • Miller OL, Jr., Beatty BR (1969) Visualization of nucleolar genes. Science 164:955–957

    Article  PubMed  Google Scholar 

  • Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91:457–466

    Article  PubMed  CAS  Google Scholar 

  • Moreno AB, Martinez de Alba AE, Bardou F, Crespi MD, Vaucheret H, Maizel A, Mallory AC (2013) Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate posttranscriptional gene silencing in plants. Nucleic Acids Res 41:4699–4708

    Article  PubMed  CAS  Google Scholar 

  • Murata Y, Wharton RP (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80:747–756

    Article  PubMed  CAS  Google Scholar 

  • Olivas W, Parker R (2000) The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. Embo J 19:6602–6611

    Article  PubMed  CAS  Google Scholar 

  • Olmedo G, Guo H, Gregory BD, Nourizadeh SD, Aguilar-Henonin L, Li H, An F, Guzman P, Ecker JR (2006) ETHYLENEINSENSITIVE5 encodes a 5′→3′ exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. Proc Natl Acad Sci USA 103:13286–13293

    Article  PubMed  CAS  Google Scholar 

  • Panasenko O, Landrieux E, Feuermann M, Finka A, Paquet N, Collart MA (2006) The yeast Ccr4-Not complex controls ubiquitination of the nascent-associated polypeptide (NAC-EGD) complex. J Biol Chem 281:31389–31398

    Article  PubMed  CAS  Google Scholar 

  • Potuschak T, Vansiri A, Binder BM, Lechner E, Vierstra RD, Genschik P (2006) The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 18:3047–3057

    Article  PubMed  CAS  Google Scholar 

  • Quenault T, Lithgow T, Traven A (2011) PUF proteins: repression, activation and mRNA localization. Trends Cell Biol 21:104–112

    Article  PubMed  CAS  Google Scholar 

  • Ren YG, Martinez J, Virtanen A (2002) Identification of the active site of poly(A)-specific ribonuclease by site-directed mutagenesis and Fe2+-mediated cleavage. J Biol Chem 277:5982–5987

    Article  PubMed  CAS  Google Scholar 

  • Reverdatto SV, Dutko JA, Chekanova JA, Hamilton DA, Belostotsky DA (2004) mRNA deadenylation by PARN is essential for embryogenesis in higher plants. RNA 10:1200–1214

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • San Paolo S, Vanacova S, Schenk L, Scherrer T, Blank D, Keller W, Gerber AP (2009) Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet 5:e1000555

    Article  PubMed  Google Scholar 

  • Sarowar S, Oh HW, Cho HS, Baek KH, Seong ES, Joung YH, Choi GJ, Lee S, Choi D (2007) Capsicum annuum CCR4-associated factor CaCAF1 is necessary for plant development and defence response. Plant J 51:792–802

    Article  PubMed  CAS  Google Scholar 

  • Schmidt K, Xu Z, Mathews DH, Butler JS (2012) Air proteins control differential TRAMP substrate specificity for nuclear RNA surveillance. Rna 18:1934–1945

    Article  PubMed  CAS  Google Scholar 

  • Smith AP, DeRidder BP, Guo WJ, Seeley EH, Regnier FE, Goldsbrough PB (2004) Proteomic analysis of Arabidopsis glutathione Stransferases from benoxacor- and copper-treated seedlings. J Biol Chem 279:26098–26104

    Article  PubMed  CAS  Google Scholar 

  • Sonoda J, Wharton RP (1999) Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 13:2704–2712

    Article  PubMed  CAS  Google Scholar 

  • Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183

    Article  PubMed  CAS  Google Scholar 

  • Suzuki A, Igarashi K, Aisaki K, Kanno J, Saga Y (2010) NANOS2 interacts with the CCR4-NOT deadenylation complex and leads to suppression of specific RNAs. Proc Natl Acad Sci USA 107: 3594–3599

    Article  PubMed  CAS  Google Scholar 

  • Suzuki A, Saba R, Miyoshi K, Morita Y, Saga Y (2012) Interaction between NANOS2 and the CCR4-NOT deadenylation complex is essential for male germ cell development in mouse. PLoS One 7:e33558

    Article  PubMed  CAS  Google Scholar 

  • Ulbricht RJ, Olivas WM (2008) Puf1p acts in combination with other yeast Puf proteins to control mRNA stability. RNA 14:246–262

    Article  PubMed  CAS  Google Scholar 

  • Vanacova S, Stefl R (2007) The exosome and RNA quality control in the nucleus. EMBO Rep 8:651–657

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Walley JW, Kelley DR, Savchenko T, Dehesh K (2010) Investigating the function of CAF1 deadenylases during plant stress responses. Plant Signal Behav 5:802–805

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Song X, Gu L, Li X, Cao S, Chu C, Cui X, Chen X, Cao X (2013) NOT2 proteins promote polymerase II-dependent transcription and interact with multiple MicroRNA biogenesis factors in Arabidopsis. Plant Cell 25:715–727

    Article  PubMed  CAS  Google Scholar 

  • Wharton RP, Aggarwal AK (2006) mRNA regulation by Puf domain proteins. Sci STKE 2006:pe37

    Article  PubMed  Google Scholar 

  • Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y (1998) The Pumilio RNA-binding domain is also a translational regulator. Mol Cell 1:863–872

    Article  PubMed  CAS  Google Scholar 

  • Wilusz CJ, Wormington M, Peltz SW (2001) The cap-to-tail guide to mRNA turnover. Nat Rev Mol Cell Biol 2:237–246

    Article  PubMed  CAS  Google Scholar 

  • Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S (1997) Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124:3015–3023

    PubMed  CAS  Google Scholar 

  • Xi L, Moscou MJ, Meng Y, Xu W, Caldo RA, Shaver M, Nettleton D, Wise RP (2009) Transcript-based cloning of RRP46, a regulator of rRNA processing and R gene-independent cell death in barley-powdery mildew interactions. Plant Cell 21:3280–3295

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Zhang B, Jia J, Yan C, Habaike A, Han Y (2013) RRP41L, a putative core subunit of the exosome, plays an important role in seed germination and early seedling growth in Arabidopsis. Plant Physiol 161:165–178

    Article  PubMed  CAS  Google Scholar 

  • Zamore PD, Williamson JR, Lehmann R (1997) The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3:1421–1433

    PubMed  CAS  Google Scholar 

  • Zhang B, Gallegos M, Puoti A, Durkin E, Fields S, Kimble J, Wickens MP (1997) A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390:477–484

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Murphy C, Sieburth LE (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc Natl Acad Sci USA 107:15981–15985

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Bioscience and Bioinformatics, Myongji University, Yongin, Kyunggi-do, 449-728, Korea

    Nazia Abbasi & Sang-Bong Choi

  2. Department of Biological Sciences, Chungnam National University, Daejeon, 305-764, Korea

    Youn-Il Park

Authors
  1. Nazia Abbasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Youn-Il Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sang-Bong Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang-Bong Choi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abbasi, N., Park, YI. & Choi, SB. RNA deadenylation and decay in plants. J. Plant Biol. 56, 198–207 (2013). https://doi.org/10.1007/s12374-013-0201-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-013-0201-8

Keywords

Search

Navigation