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Interconnections between mRNA degradation and RDR-dependent siRNA production in mRNA turnover in plants

  • JPR Symposium
  • Expanding plant non-coding RNA world
  • Published:
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Abstract

Accumulation of an mRNA species is determined by the balance between the synthesis and the degradation of the mRNA. Individual mRNA molecules are selectively and actively degraded through RNA degradation pathways, which include 5′-3′ mRNA degradation pathway, 3′-5′ mRNA degradation pathway, and RNA-dependent RNA polymerase-mediated mRNA degradation pathway. Recent studies have revealed that these RNA degradation pathways compete with each other in mRNA turnover in plants and that plants have a hidden layer of non-coding small-interfering RNA production from a set of mRNAs. In this review, we summarize the current information about plant mRNA degradation pathways in mRNA turnover and discuss the potential roles of a novel class of the endogenous siRNAs derived from plant mRNAs.

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Abbreviations

AGO:

Argonaute

CAF1:

CCR4-associated factor 1

CCR4:

Carbon catabolite repressor 4

ct-siRNA:

Coding transcript-derived siRNA

DCL:

Dicer-like

DCP:

Decapping protein

dsRNA:

Double-stranded RNA

miRNA:

MicroRNA

nt:

nucleotide

PARN:

Poly(A) ribonuclease

P-body:

Processing body

phasiRNA:

Phased, secondary siRNA

PTGS:

Post-transcriptional gene silencing

RDR:

RNA-dependent RNA polymerase

rqc-siRNA:

RNA quality control-siRNA

SGS3:

Suppressor of gene silencing 3

siRNA:

Small-interfering RNA

SKI:

Superkiller

tasiRNA:

Trans-acting siRNA

TGS:

Transcriptional gene silencing

TRAMP:

Trf4p/Air2p/Mtr4p polyadenylation

vasiRNA:

Virus-activated siRNA

VCS:

Varicose

XRN:

5′-3′ exoribonuclease

References

  • Allen RS, Li J, Stahle MI, Dubroué A, Gubler F, Millar A (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci USA 104:16371–16376

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JS, Parker RP (1998) The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J 17:1497–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barreau C, Paillard L, Osborne HB (2006) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33:7138–7150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonneau F, Basquin J, Ebert J, Lorentzen E, Conti E (2009) The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139:547–559

    Article  CAS  PubMed  Google Scholar 

  • Bouché N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25:3347–3356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Branscheid A, Marchais A, Schott G, Lange H, Gagliardi D, Andersen SU, Voinnet O, Brodersen P (2015) SKI2 mediates degradation of RISC 5′-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis. Nucleic Acids Res 43:10975–10988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brengues M, Teixeira D, Parker R (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310:486–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briggs MW, Burkard TDB, Butler JS (1998) Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J Biol Chem 273:13255–13263

    Article  CAS  PubMed  Google Scholar 

  • Brown J, Bai X (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6:449–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao M, Du P, Wang X, Yu YQ, Qiu YH, Li W, Gal-On A, Zhou C, Li Y, Ding SW (2014) Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis. Proc Natl Acad Sci USA 111:14613–14618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang JH, Jiao X, Chiba K, Oh C, Martin CE, Kiledjian M, Tong L (2012) Dxo1 is a new type of eukaryotic enzyme with both decapping and 5′-3′ exoribonuclease activity. Nat Struct Mol Biol 19:1011–1017

    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 5.8 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  CAS  PubMed  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) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131:1340–1353

    Article  CAS  PubMed  Google Scholar 

  • Chen CA, Shyu AB (2017) Emerging themes in regulation of global mRNA turnover in cis. Trends Biochem Sci 42:16–27

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Chlebowski A, Lubas M, Jensen TH, Dziembowski A (2013) RNA decay machines: the exosome. Biochim Biophys Acta 1829:552–560

    Article  CAS  PubMed  Google Scholar 

  • Cho SH, Coruh C, Axtell MJ (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24:4837–4849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christie M, Brosnan CA, Rothnagel JA, Carroll BJ (2011) RNA decay and RNA silencing in plants: competition or collaboration? Front Plant Sci 2:99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui P, Zhang S, Ding F, Ali S, Xiong L (2014) Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis. Genome Biol 15:R1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Derrien B, Baumberger N, Schepetilnikov M, Viotti C, Cillia J De Ziegler-Graffa V, Isonoc E, Schumacherb K, Genschik P (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci USA 109:15942–15946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Zhao Y, He J, Zhang Y, Xi H, Liu M, Ma J, Wu L (2016) YTHDF2 destabilizes m(6)A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nat Commun 25:12626

    Article  CAS  Google Scholar 

  • Dunckley T, Parker R (1999) The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 18:5411–5422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938

    Article  CAS  PubMed  Google Scholar 

  • Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15:1494–1500

    Article  CAS  PubMed  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  CAS  PubMed  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 

  • Golisz A, Sikorski PJ, Kruszka K, Kufel J (2013) Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation. Nucleic Acids Res 41:6232–6249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory BD, O’Malley RC, Lister R, Urich MA, Tonti-Filippini J, Chen H, Millar AH, Ecker JR (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev Cell 14:854–866

    Article  CAS  PubMed  Google Scholar 

  • Gunawardana D, Cheng HC, Gayler KR (2008) Identification of functional domains in Arabidopsis thaliana mRNA decapping enzyme (AtDcp2). Nucleic Acids Res 36:203–216

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Halbach F, Reichelt P, Rode M, Conti E (2013) The yeast Ski complex: Crystal structure and RNA channeling to the exosome complex. Cell 154:814–826

    Article  CAS  PubMed  Google Scholar 

  • Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y, Hashimoto T, Baskin TI (2012) RNA processing bodies, peroxisomes, golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 53:699–708

    Article  CAS  PubMed  Google Scholar 

  • Hayashi M, Nanba C, Saito M, Kondo M, Takeda A, Watanabe Y, Nishimura M (2012) Loss of XRN4 function can trigger cosuppression in a sequence-dependent manner. Plant Cell Physiol 53:1310–1321

    Article  CAS  PubMed  Google Scholar 

  • Heyer WD, Johnson AW, Reinhart U, Kolodner RD (1995) Regulation and intracellular localization of Saccharomyces cerevisiae strand exchange protein 1 (Sep1/Xrn1/Kem1), a multifunctional exonuclease. Mol Cell Biol 15:2728–2736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Howell MD, Fahlgren N, Chapman EJ, Cumbie JS, Sullivan CM, Givan SA, Kasschau KD, Carrington JC (2007) Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell 19:926–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwakawa HO, Tomari Y (2013) Molecular insights into microRNA-mediated translational repression in plants. Mol Cell 52:591–601

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki S, Takeda A, Motose H, Watanabe Y (2007) Characterization of Arabidopsis decapping proteins AtDCP1 and AtDCP2, which are essential for post-embryonic development. FEBS Lett 581:2455–2459

    Article  CAS  PubMed  Google Scholar 

  • Jiao X, Xiang S, Oh C, Martin CE, Tong L, Kiledjian M (2010) Identification of a quality-control mechanism for mRNA 5′-end capping. Nature 467:608–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson MA, Perez-Amador MA, Lidder P, Green PJ (2000) Mutants of Arabidopsis defective in a sequence-specific mRNA degradation pathway. Proc Natl Acad Sci USA 97:13991–13996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jouannet V, Moreno AB, Elmayan T, Vaucheret H, Crespi MD, Maizel A (2012) Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J 31:1704–1713

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R, Watanabe Y (2009) SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett 583:1261–1266

    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 

  • Kumakura N, Otsuki H, Ito M, Nomoto M, Tada Y, Ohta K, Watanabe Y (2016) Arabidopsis AtRRP44 has ribonuclease activity that is required to complement the growth defect of yeast rrp44 mutant. Plant Biotech 33:77–85

    Article  CAS  Google Scholar 

  • Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • LaGrandeur TE, Parker R (1998) Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J 17:1487–1496

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Lange H, Zuber H, Sement FM, Chicher J, Kuhn L, Hammann P, Brunaud V, Bérard C, Bouteiller N, Balzergue S, Aubourg S, Martin-Magniette M-L, Vaucheret H, Gagliardi D (2014) The RNA helicases AtMTR4 and HEN2 target specific subsets of nuclear transcripts for degradation by the nuclear exosome in Arabidopsis thaliana. PLoS Genet 10:e1004564

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lebreton A, Tomecki R, Dziembowski A, Séraphin B (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456:993–996

    Article  CAS  PubMed  Google Scholar 

  • Li C, Zhang B (2016) MicroRNAs in control of plant development. J Cell Physiol 231:303–313

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Ho ES, Gunderson SI, Kiledjian M (2009) Mutational analysis of a Dcp2-binding element reveals general enhancement of decapping by 5′-end stem-loop structures. Nucleic Acids Res 37:2227–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Ma M, Feng Y, Li H, Wang Y, Ma Y, Li M, An F, Guo H (2015) EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell 163:670–683

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

    Article  CAS  PubMed  Google Scholar 

  • Lorentzen E, Basquin J, Tomecki R, Dziembowski A, Conti E (2008) Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol Cell 29:717–728

    Article  CAS  PubMed  Google Scholar 

  • Lubas M, Christensen MS, Kristiansen MS, Domanski M, Falkenby LG, Lykke-Andersen S, Andersen JS, Dziembowski A, Jensen TH (2011) Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43:624–637

    Article  CAS  PubMed  Google Scholar 

  • Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lykke-Andersen J (2002) Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 22:8114–8121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A (2011) The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8:61–66

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Martínez de Alba AE, Moreno AB, Gabriel M, Mallory AC, Christ A, Bounon R, Balzergue S, Aubourg S, Gautheret D, Crespi MD, Vaucheret H, Maizel A (2015) In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Res 43:2902–2913

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  PubMed  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 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008a) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141

    Article  CAS  PubMed  Google Scholar 

  • Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH, Carrington JC (2008b) AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci USA 105:20055–20062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon SL, Blackinton JG, Anderson JR, Dozier MK, Dodd BJ, Keene JD, Wilusz CJ, Bradrick SS, Wilusz J (2015) XRN1 stalling in the 5′ UTR of Hepatitis C virus and Bovine Viral Diarrhea virus is associated with dysregulated host mRNA stability. PLoS Pathog 11:e1004708

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moreno AB, Martínez 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 post-transcriptional gene silencing in plants. Nucleic Acids Res 41:4699–4708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motomura K, Le QT, Kumakura N, Fukaya T, Takeda A, Watanabe Y (2012) The role of decapping proteins in the miRNA accumulation in Arabidopsis thaliana. RNA Biol 9:644–652

    Article  CAS  PubMed  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 

  • Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Rémoué K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542

    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 

  • 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 

  • Nishimura N, Kitahata N, Seki M, Narusaka Y, Narusaka M, Kuromori T, Asami T, Shinozaki K, Hirayama T (2005) Analysis of ABA hypersensitive germination 2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984

    Article  CAS  PubMed  Google Scholar 

  • Okamoto M, Matsui A, Tanaka M, Morosawa T, Ishida J, Iida K, Mochizuki Y, Toyoda T, Seki M (2016) Sm-like protein-mediated RNA metabolism is required for heat stress tolerance in Arabidopsis. Front Plant Sci 7:1079

    Article  PubMed  PubMed Central  Google Scholar 

  • Olmedo G, Guo H, Gregory BD, Nourizadeh SD, Aguilar-Henonin L, Li H, An F, Guzman P, Ecker JR (2006) ETHYLENE-INSENSITIVE5 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    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 

  • Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perea-Resa C, Hernández-Verdeja T, López-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-López C, Catalá R, Turečková V, Novak O, Zhang W, Sieburth L, Jiménez-Gómez 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-Santángelo S, Mancini E, Francey LJ, Schlaen RG, Chernomoretz A, Hogenesch JB, Yanovsky MJ (2014) Role for LSM genes in the regulation of circadian rhythms. Proc Natl Acad Sci USA 111:15166–15171

    Article  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu J, Kang SG, Wang W, Musier-Forsyth K, Jang JC (2014) The Arabidopsis thaliana tandem zinc finger 1 (AtTZF1) protein in RNA binding and decay. Plant J 78:452–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radhakrishnan A, Chen YH, Martin S, Alhusaini N, Green R, Coller J (2016) The DEAD-box protein Dhh1p couples mRNA decay and translation by monitoring codon optimality. Cell 167:122–132

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux ME, Rasmussen MW, Palma K, Lolle S, Regué ÀM, Bethke G, Glazebrook J, Zhang W, Sieburth L, Larsen MR, Mundy J, Petersen M (2015) The mRNA decay factor PAT1 functions in a pathway including MAP kinase 4 and immune receptor SUMM2. EMBO J 34:593–608

    Article  CAS  PubMed  PubMed Central  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 

  • Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A (2008) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struc. Mol Biol 16:56–62

    Google Scholar 

  • Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491

    Article  CAS  PubMed  Google Scholar 

  • Shin J-H, Chekanova JA (2014) Arabidopsis RRP6L1 and RRP6L2 function in FLOWERING LOCUS C silencing via regulation of antisense RNA synthesis. PLOS Genet 10:e1004612

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song MG, Li Y, Kiledjian M (2010) Multiple mRNA decapping enzymes in mammalian cells. Mol Cell 40:423–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song MG, Bail S, Kiledjian M (2013) Multiple Nudix family proteins possess mRNA decapping activity. RNA 19:390–399

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  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 

  • Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49:493–500

    Article  CAS  PubMed  Google Scholar 

  • Thran M, Link K, Sonnewald U (2012) The Arabidopsis DCP2 gene is required for proper mRNA turnover and prevents transgene silencing in Arabidopsis. Plant J 72:368–377

    Article  CAS  PubMed  Google Scholar 

  • Trcek T, Larson DR, Moldón A, Query CC, Singer RH (2011) Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 147:1484–1497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuzuki M, Nishihama R, Ishizaki K, Kurihara Y, Matsui M, Bowman JL, Kohchi T, Hamada T, Watanabe Y (2016) Profiling and characterization of small RNAs in the liverwort, Marchantia polymorpha, belonging to the first diverged land plants. Plant Cell Physiol 57:359–372

    Article  CAS  PubMed  Google Scholar 

  • Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R (2001) The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104:377–386

    Article  CAS  PubMed  Google Scholar 

  • van Dijk E, Cougot N, Meyer S, Babajko S, Wahle E, Séraphin B (2002) Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21:6915–6924

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogel F, Hofius D, Paulus KE, Jungkunz I, Sonnewald U (2011) The second face of a known player: Arabidopsis silencing suppressor AtXRN4 acts organ-specifically. New Phytol 189:484–493

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci 13:317–328

    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 W, Ye R, Xin Y, Fang X, Li C, Shi H, Zhou X, Qi Y (2011) An importin β protein negatively regulates microRNA activity in Arabidopsis. Plant Cell 23:3565–3576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G, Ren B, Pan T, He C (2014) N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505:117–120

    Article  PubMed  CAS  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 

  • 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  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 (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 

  • Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB (2005) Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12:1054–1063

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Yu A, Saudemont B, Bouteiller N, Elvira-Matelot E, Lepère G, Parent JS, Morel JB1, Cao J, Elmayan T, Vaucheret H (2015) Second-site mutagenesis of a hypomorphic argonaute1 allele identifies SUPERKILLER3 as an endogenous suppressor of transgene posttranscriptional gene silencing. Plant Physiol 169:1266–1274

    Article  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Zhang S, Zhang Y, Wang X, Li D, Li Q, Yue M, Li Q, Zhang YE, Xu Y, Xue Y, Chong K, Bao S (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23:396–411

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Tang K, Qian W, Duan CG, Wang B, Zhang H, Wang P, Zhu X, Lang Z, Yang Y, Zhu JK (2014) An Rrp6-like protein positively regulates noncoding RNA levels and DNA methylation in Arabidopsis. Mol Cell 54:418–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhu Y, Liu X, Hong X, Xu Y, Zhu P, Shen Y, Wu H, Ji Y, Wen X, Zhang C, Zhao Q, Wang Y, Lu J, Guo H (2015) Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis. Science 348:120–123

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Kunst L (2016) SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems. Plant Physiol 171:960–973

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Editage (http://www.editage.jp) for English language editing. This work was supported by JSPS KAKENHI Grant Numbers (15J08774 to M.T., 16J02257 to K.M., 15K14665, 26712006, 16H04882, and 16H04883 to A.T.) and The Kato Memorial Bioscience Foundation (to A.T.).

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Authors and Affiliations

  1. Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, 153-8902, Japan

    Masayuki Tsuzuki

  2. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, 48109, USA

    Masayuki Tsuzuki

  3. Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Kazuki Motomura

  4. Center for Sustainable Resource Science, RIKEN, Suehiro-cho 1-7-22, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Naoyoshi Kumakura

  5. Department of Biotechnology, Graduate School of Life Sciences, Ritsumeikan University, Shiga, 525–8577, Japan

    Atsushi Takeda

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  1. Masayuki Tsuzuki
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  2. Kazuki Motomura
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  4. Atsushi Takeda
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Correspondence to Atsushi Takeda.

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Tsuzuki, M., Motomura, K., Kumakura, N. et al. Interconnections between mRNA degradation and RDR-dependent siRNA production in mRNA turnover in plants. J Plant Res 130, 211–226 (2017). https://doi.org/10.1007/s10265-017-0906-8

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