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Journal of Plant Research

, Volume 130, Issue 2, pp 211–226 | Cite as

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

  • Masayuki Tsuzuki
  • Kazuki Motomura
  • Naoyoshi Kumakura
  • Atsushi Takeda
JPR Symposium Expanding plant non-coding RNA world

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.

Keywords

Coding transcript-derived siRNA 3′-5′ mRNA degradation 5′-3′ mRNA degradation mRNA turnover RNA exosome RNA-dependent RNA polymerase RNA quality control-siRNA RNA silencing Virus-activated siRNA 

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

Notes

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.).

References

  1. 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 104:16371–16376PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 13:2148–2158PubMedPubMedCentralCrossRefGoogle Scholar
  3. 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 17:1497–1506PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barreau C, Paillard L, Osborne HB (2006) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33:7138–7150PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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 17:170–180PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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 139:547–559PubMedCrossRefGoogle Scholar
  7. 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 25:3347–3356PubMedPubMedCentralCrossRefGoogle Scholar
  8. 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 43:10975–10988PubMedPubMedCentralCrossRefGoogle Scholar
  9. Brengues M, Teixeira D, Parker R (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310:486–489PubMedPubMedCentralCrossRefGoogle Scholar
  10. 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 273:13255–13263PubMedCrossRefGoogle Scholar
  11. Brown J, Bai X (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6:449–457PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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 111:14613–14618PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 19:1011–1017PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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 275:33158–33166PubMedCrossRefGoogle Scholar
  15. 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 131:1340–1353PubMedCrossRefGoogle Scholar
  16. Chen CA, Shyu AB (2017) Emerging themes in regulation of global mRNA turnover in cis. Trends Biochem Sci 42:16–27PubMedCrossRefGoogle Scholar
  17. Chiba Y, Johnson MA, Lidder P, Vogel JT, van Erp H, Green PJ (2004) AtPARN is an essential poly(A) ribonuclease in Arabidopsis. Gene 328:95–102PubMedCrossRefGoogle Scholar
  18. Chlebowski A, Lubas M, Jensen TH, Dziembowski A (2013) RNA decay machines: the exosome. Biochim Biophys Acta 1829:552–560PubMedCrossRefGoogle Scholar
  19. Cho SH, Coruh C, Axtell MJ (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24:4837–4849PubMedPubMedCentralCrossRefGoogle Scholar
  20. Christie M, Brosnan CA, Rothnagel JA, Carroll BJ (2011) RNA decay and RNA silencing in plants: competition or collaboration? Front Plant Sci 2:99PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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:R1PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 109:15942–15946PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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 25:12626CrossRefGoogle Scholar
  24. Dunckley T, Parker R (1999) The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 18:5411–5422PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 14:15–22PubMedCrossRefGoogle Scholar
  26. Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415PubMedPubMedCentralCrossRefGoogle Scholar
  27. Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938PubMedCrossRefGoogle Scholar
  28. 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 15:1494–1500PubMedCrossRefGoogle Scholar
  29. Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–1048PubMedCrossRefGoogle Scholar
  30. 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 19:1549–1564PubMedPubMedCentralCrossRefGoogle Scholar
  31. Golisz A, Sikorski PJ, Kruszka K, Kufel J (2013) Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation. Nucleic Acids Res 41:6232–6249PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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 14:854–866PubMedCrossRefGoogle Scholar
  33. Gunawardana D, Cheng HC, Gayler KR (2008) Identification of functional domains in Arabidopsis thaliana mRNA decapping enzyme (AtDcp2). Nucleic Acids Res 36:203–216PubMedCrossRefGoogle Scholar
  34. 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 19:3451–3461PubMedPubMedCentralCrossRefGoogle Scholar
  35. Halbach F, Reichelt P, Rode M, Conti E (2013) The yeast Ski complex: Crystal structure and RNA channeling to the exosome complex. Cell 154:814–826PubMedCrossRefGoogle Scholar
  36. 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 53:699–708PubMedCrossRefGoogle Scholar
  37. 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 53:1310–1321PubMedCrossRefGoogle Scholar
  38. 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 15:2728–2736PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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 4:2247Google Scholar
  40. 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 19:904–913PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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 19:926–942PubMedPubMedCentralCrossRefGoogle Scholar
  42. Iwakawa HO, Tomari Y (2013) Molecular insights into microRNA-mediated translational repression in plants. Mol Cell 52:591–601PubMedCrossRefGoogle Scholar
  43. 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 581:2455–2459PubMedCrossRefGoogle Scholar
  44. 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 467:608–611PubMedPubMedCentralCrossRefGoogle Scholar
  45. 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 97:13991–13996PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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 31:1704–1713PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 97:13985–13990PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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 583:1261–1266PubMedCrossRefGoogle Scholar
  49. 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:e79219PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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 33:77–85CrossRefGoogle Scholar
  51. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758PubMedPubMedCentralCrossRefGoogle Scholar
  52. LaCava J, Houseley J, Saveanu C, Petfalski E (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713–724PubMedCrossRefGoogle Scholar
  53. LaGrandeur TE, Parker R (1998) Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J 17:1487–1496PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 159:1385–1395PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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 28:3038–3044PubMedPubMedCentralCrossRefGoogle Scholar
  56. 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 68:51–63PubMedCrossRefGoogle Scholar
  57. 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:e1004564PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lebreton A, Tomecki R, Dziembowski A, Séraphin B (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456:993–996PubMedCrossRefGoogle Scholar
  59. Li C, Zhang B (2016) MicroRNAs in control of plant development. J Cell Physiol 231:303–313PubMedCrossRefGoogle Scholar
  60. 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 37:2227–2237PubMedPubMedCentralCrossRefGoogle Scholar
  61. 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 163:670–683PubMedCrossRefGoogle Scholar
  62. 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 19:307–316PubMedCrossRefGoogle Scholar
  63. Liu L, Chen X (2016) RNA quality control as a key to suppressing RNA silencing of endogenous genes in plants. Mol Plant 9:826–836PubMedPubMedCentralCrossRefGoogle Scholar
  64. Liu Q, Greimann JC, Lima CD (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127:1223–1237PubMedCrossRefGoogle Scholar
  65. 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 29:717–728PubMedCrossRefGoogle Scholar
  66. 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 43:624–637PubMedCrossRefGoogle Scholar
  67. Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–958PubMedPubMedCentralCrossRefGoogle Scholar
  68. Lykke-Andersen J (2002) Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 22:8114–8121PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A (2011) The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8:61–66PubMedCrossRefGoogle Scholar
  70. Makino DL, Baumgärtner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495:70–75PubMedCrossRefGoogle Scholar
  71. 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 43:2902–2913PubMedPubMedCentralCrossRefGoogle Scholar
  72. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408PubMedCrossRefGoogle Scholar
  73. 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 5:1279–1293PubMedCrossRefGoogle Scholar
  74. 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 133:116–127PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 133:128–141PubMedCrossRefGoogle Scholar
  76. 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 105:20055–20062PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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:e1004708PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 41:4699–4708PubMedPubMedCentralCrossRefGoogle Scholar
  79. 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 9:644–652PubMedCrossRefGoogle Scholar
  80. 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 56:107–115PubMedCrossRefGoogle Scholar
  81. 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 101:533–542PubMedCrossRefGoogle Scholar
  82. Nagarajan VK, Jones CI, Newbury SF, Green PJ (2013) XRN 5′→3′ exoribonucleases: structure, mechanisms and functions. Biochim Biophys Acta 1829:590–603PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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 56:1762–1772PubMedCrossRefGoogle Scholar
  84. 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 44:972–984PubMedCrossRefGoogle Scholar
  85. 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 7:1079PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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 103:13286–13293PubMedPubMedCentralCrossRefGoogle Scholar
  87. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  88. Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646PubMedCrossRefGoogle Scholar
  89. 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 18:2368–2379PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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 24:4930–4947PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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 28:505–520PubMedPubMedCentralCrossRefGoogle Scholar
  92. 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 111:15166–15171PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 18:3047–3057PubMedPubMedCentralCrossRefGoogle Scholar
  94. 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 78:452–467PubMedPubMedCentralCrossRefGoogle Scholar
  95. 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 167:122–132PubMedPubMedCentralCrossRefGoogle Scholar
  96. Reverdatto SV, Dutko JA, Chekanova JA, Hamilton DA, Belostotsky DA (2004) mRNA deadenylation by PARN is essential for embryogenesis in higher plants. RNA 10:1200–1214PubMedPubMedCentralCrossRefGoogle Scholar
  97. 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 34:593–608PubMedPubMedCentralCrossRefGoogle Scholar
  98. 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 17:501–511PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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 16:56–62Google Scholar
  100. Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491PubMedCrossRefGoogle Scholar
  101. 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:e1004612PubMedPubMedCentralCrossRefGoogle Scholar
  102. Song MG, Li Y, Kiledjian M (2010) Multiple mRNA decapping enzymes in mammalian cells. Mol Cell 40:423–432PubMedPubMedCentralCrossRefGoogle Scholar
  103. Song MG, Bail S, Kiledjian M (2013) Multiple Nudix family proteins possess mRNA decapping activity. RNA 19:390–399PubMedPubMedCentralCrossRefGoogle Scholar
  104. Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183PubMedCrossRefGoogle Scholar
  105. 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 56:863–874PubMedCrossRefGoogle Scholar
  106. 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 49:493–500PubMedCrossRefGoogle Scholar
  107. 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 72:368–377PubMedCrossRefGoogle Scholar
  108. Trcek T, Larson DR, Moldón A, Query CC, Singer RH (2011) Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 147:1484–1497PubMedPubMedCentralCrossRefGoogle Scholar
  109. 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 57:359–372PubMedCrossRefGoogle Scholar
  110. 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 104:377–386PubMedCrossRefGoogle Scholar
  111. 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 21:6915–6924PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 189:484–493PubMedCrossRefGoogle Scholar
  113. Voinnet O (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci 13:317–328PubMedCrossRefGoogle Scholar
  114. 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 152:866–875PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 23:3565–3576PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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 505:117–120PubMedCrossRefGoogle Scholar
  117. Weber C, Nover L, Fauth M (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56:517–530PubMedCrossRefGoogle Scholar
  118. 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 1:771–781PubMedCrossRefGoogle Scholar
  119. Xu J, Chua NH (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell 21:3270–3279PubMedPubMedCentralCrossRefGoogle Scholar
  120. Xu J, Chua NH (2012) Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO J 31:1975–1984PubMedPubMedCentralCrossRefGoogle Scholar
  121. Xu J, Yang JY, Niu QW, Chua NH (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18:3386–3398PubMedPubMedCentralCrossRefGoogle Scholar
  122. 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 12:1054–1063PubMedCrossRefGoogle Scholar
  123. 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 161:165–178PubMedCrossRefGoogle Scholar
  124. 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 169:1266–1274PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 107:15981–15985PubMedPubMedCentralCrossRefGoogle Scholar
  126. 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 23:396–411PubMedPubMedCentralCrossRefGoogle Scholar
  127. 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 54:418–430PubMedPubMedCentralCrossRefGoogle Scholar
  128. 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 348:120–123PubMedCrossRefGoogle Scholar
  129. 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 171:960–973PubMedPubMedCentralGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of Life SciencesGraduate School of Arts and Sciences, The University of TokyoTokyoJapan
  2. 2.Department of Molecular, Cellular and Developmental BiologyUniversity of MichiganAnn ArborUSA
  3. 3.Institute of Transformative Bio-Molecules, Nagoya UniversityNagoyaJapan
  4. 4.Center for Sustainable Resource Science, RIKENYokohamaJapan
  5. 5.Department of BiotechnologyGraduate School of Life Sciences, Ritsumeikan UniversityShigaJapan

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