Distinct 18S rRNA precursors are targets of the exosome complex, the exoribonuclease RRP6L2 and the terminal nucleotidyltransferase TRL in Arabidopsis thaliana

Plant Journal

Volumn 83, Issue 6, 2015, Pages 991-1004

  Sikorski, Pawel J ^a,b   Zuber, Hélène ^a   Philippe, Lucas ^a   Sement, François M ^a   Canaday, Jean ^a   Kufel, Joanna ^b   Gagliardi, Dominique ^a   Lange, Heike ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF WARSAW   (Poland)

Author keywords

18S rRNA processing; Arabidopsis thaliana; polyadenylation; RNA exosome; RRP6L2; terminal nucleotidyltransferase; uridylation

Indexed keywords

BIOCHEMISTRY; DATA HANDLING; NUCLEIC ACIDS;

18S RRNA; ARABIDOPSIS THALIANA; POLYADENYLATION; RRP6L2; URIDYLATION;

RNA;

ARABIDOPSIS PROTEIN; EXORIBONUCLEASE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; NUCLEAR PROTEIN; NUCLEOTIDYLTRANSFERASE; RNA 18S; RNA PRECURSOR; RRP6L2 PROTEIN, ARABIDOPSIS; TRL PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; GENETICS; METABOLISM; PHYLOGENY; RNA PROCESSING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; NUCLEAR PROTEINS; NUCLEOTIDYLTRANSFERASES; PHYLOGENY; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL, 18S;

EID: 84941120550     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12943     Document Type: Article

References (73)

1. Allmang, C., Mitchell, P., Petfalski, E., and, Tollervey, D., (2000) Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 28, 1684-1691.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al,. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
3. Armistead, J., and, Triggs-Raine, B., (2014) Diverse diseases from a ubiquitous process: the ribosomopathy paradox. FEBS Lett. 588, 1491-1500.
4. Bernstein, K.A., Gallagher, J.E.G., Mitchell, B.M., Granneman, S., and, Baserga, S.J., (2004) The small-subunit processome is a ribosome assembly intermediate. Eukaryot. Cell, 3, 1619-1626.
5. Byrne, M.E., (2009) A role for the ribosome in development. Trends Plant Sci. 14, 512-519.
6. Carron, C., O'Donohue, M.-F., Choesmel, V., Faubladier, M., and, Gleizes, P.-E., (2011) Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic Acids Res. 39, 280-291.
7. Chang, H.-M., Triboulet, R., Thornton, J.E., and, Gregory, R.I., (2013) A role for the Perlman syndrome exonuclease Dis3 l2 in the Lin28-let-7 pathway. Nature, 497, 244-248.
8. Chekanova, J.A., Gregory, B.D., Reverdatto, S.V., et al. (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell, 131, 1340-1353.
9. Chevenet, F., Brun, C., Bañuls, A.-L., Jacq, B., and, Christen, R., (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. Bioinformatics, 7, 439.
10. Comella, P., Pontvianne, F., Lahmy, S., Vignols, F., Barbezier, N., Debures, A., Jobet, E., Brugidou, E., Echeverria, M., and, Sáez-Vásquez, J., (2008) Characterization of a ribonuclease III-like protein required for cleavage of the pre-rRNA in the 3′ ETS in Arabidopsis. Nucleic Acids Res. 36, 1163-1175.
11. Dereeper, A., Guignon, V., Blanc, G., et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469.
12. Dragon, F., Gallagher, J.E., Compagnone-Post, P.A., et al. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature, 417, 967-970.
13. Ebersberger, I., Simm, S., Leisegang, M.S., Schmitzberger, P., Mirus, O., von Haeseler, A., Bohnsack, M.T., and, Schleiff, E., (2014) The evolution of the ribosome biogenesis pathway from a yeast perspective. Nucleic Acids Res. 42, 1509-1523.
14. Fatica, A., Oeffinger, M., Dlakic, M., and, Tollervey, D., (2003) Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol. Cell. Biol. 23, 1798-1807.
15. Guindon, S., and, Gascuel, O., (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
16. Gy, I., Gasciolli, V., Lauressergues, D., Morel, J.-B., Gombert, J., Proux, F., Proux, C., Vaucheret, H., and, Mallory, A.C., (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell, 19, 3451-3461.
17. Hadjiolova, K.V., Nicoloso, M., Mazan, S., Hadjiolov, A.A., and, Bachellerie, J.P., (1993) Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. Eur. J. Biochem. 212, 211-215.
18. Hang, R., Liu, C., Ahmad, A., Zhang, Y., Lu, F., and, Cao, X., (2014) Arabidopsis protein arginine methyltransferase 3 is required for ribosome biogenesis by affecting precursor ribosomal RNA processing. Proc. Natl Acad. Sci. 111, 16190-16195.
19. Henras, A.K., Plisson-Chastang, C., O'Donohue, M.-F., Chakraborty, A., and, Gleizes, P.-E., (2015) An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip. Rev. RNA, 6, 225-242.
20. Hirayama, T., Matsuura, T., Ushiyama, S., et al. (2013) A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis. Nat. Commun. 4, 2247.
21. Ibrahim, F., Rymarquis, L.A., Kim, E.-J., Becker, J., Balassa, E., Green, P.J., and, Cerutti, H., (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl Acad. Sci. 107, 3906-3911.
22. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
23. Kos, M., and, Tollervey, D., (2010) Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell, 37, 809-820.
24. Kumakura, N., Otsuki, H., Tsuzuki, M., Takeda, A., and, 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.
25. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A., and, Tollervey, D., (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell, 121, 713-724.
26. Lafontaine, D.L.J., (2010) A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem. Sci. 35, 267-277.
27. Lange, H., Holec, S., Cognat, V., Pieuchot, L., Le Ret, M., Canaday, J., and, 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.
28. Lange, H., Sement, F.M., Canaday, J., and, Gagliardi, D., (2009) Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci. 14, 497-504.
29. Lange, H., Sement, F.M., and, 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.
30. Lange, H., Zuber, H., Sement, F.M., et al. (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.
31. Lehrbach, N.J., Armisen, J., Lightfoot, H.L., Murfitt, K.J., Bugaut, A., Balasubramanian, S., and, Miska, E.A., (2009) LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 16, 1016-1020.
32. Lim, J., Ha, M., Chang, H., Kwon, S.C., Simanshu, D.K., Patel, D.J., and, Kim, V.N., (2014) Uridylation by TUT4 and TUT7 marks mRNA for degradation. Cell, 159, 1365-1376.
33. Liu, X., Zheng, Q., Vrettos, N., Maragkakis, M., Alexiou, P., Gregory, B.D., and, Mourelatos, Z., (2014) A microRNA precursor surveillance system in quality control of microRNA synthesis. Mol. Cell, 55, 868-879.
34. Lubas, M., Christensen, M.S., Kristiansen, M.S., Domanski, M., Falkenby, L.G., Lykke-Andersen, S., Andersen, J.S., Dziembowski, A., and, Jensen, T.H., (2011) Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell, 43, 624-637.
35. Lubas, M., Damgaard, C.K., Tomecki, R., Cysewski, D., Jensen, T.H., and, Dziembowski, A., (2013) Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA. EMBO J. 32, 1855-1868.
36. Malecki, M., Viegas, S.C., Carneiro, T., Golik, P., Dressaire, C., Ferreira, M.G., and, Arraiano, C.M., (2013) The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J. 32, 1842-1854.
37. Mansour, F.H., and, Pestov, D.G., (2013) Separation of long RNA by agarose-formaldehyde gel electrophoresis. Anal. Biochem. 441, 18-20.
38. Missbach, S., Weis, B.L., Martin, R., Simm, S., Bohnsack, M.T., and, Schleiff, E., (2013) 40S ribosome biogenesis co-factors are essential for gametophyte and embryo development. PLoS ONE, 8, e54084.
39. Moreno, A.B., Martínez de Alba, A.E., Bardou, F., Crespi, M.D., Vaucheret, H., Maizel, A., and, Mallory, A.C., (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.
40. Mullen, T.E., and, Marzluff, W.F., (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev. 22, 50-65.
41. Mullineux, S.-T., and, Lafontaine, D.L.J., (2012) Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie, 94, 1521-1532.
42. Norbury, C.J., (2010) 3′ Uridylation and the regulation of RNA function in the cytoplasm. Biochem. Soc. Trans. 38, 1150-1153.
43. Preti, M., O'Donohue, M.-F., Montel-Lehry, N., Bortolin-Cavaillé, M.-L., Choesmel, V., and, Gleizes, P.-E., (2013) Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA. Nucleic Acids Res. 41, 4709-4723.
44. Rammelt, C., Bilen, B., Zavolan, M., and, Keller, W., (2011) PAPD5, a noncanonical poly(A) polymerase with an unusual RNA-binding motif. RNA, 17, 1737-1746.
45. Ren, G., Chen, X., and, Yu, B., (2012) Uridylation of miRNAs by HEN1 SUPPRESSOR1 in Arabidopsis. Curr. Biol. 22, 695-700.
46. Ren, G., Xie, M., Zhang, S., Vinovskis, C., Chen, X., and, Yu, B., (2014) Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage. Proc. Natl Acad. Sci. 111, 6365-6370.
47. Rissland, O.S., and, Norbury, C.J., (2009) Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover. Nat. Struct. Mol. Biol. 16, 616-623.
48. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and, Weisshaar, B., (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53, 247-259.
49. Rouquette, J., Choesmel, V., and, Gleizes, P.-E., (2005) Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J. 24, 2862-2872.
50. Saez-Vasquez, J., Caparros-Ruiz, D., Barneche, F., and, Echeverria, M., (2004) A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro. Mol. Cell. Biol. 24, 7284-7297.
51. Samaha, H., Delorme, V., Pontvianne, F., Cooke, R., Delalande, F., Van Dorsselaer, A., Echeverria, M., and, Sáez-Vásquez, J., (2010) Identification of protein factors and U3 snoRNAs from a Brassica oleracea RNP complex involved in the processing of pre-rRNA. Plant J. 61, 383-398.
52. Sement, F.M., and, Gagliardi, D., (2014) Detection of uridylated mRNAs. Methods Mol. Biol. 1125, 43-51.
53. Sement, F.M., Ferrier, E., Zuber, H., Merret, R., Alioua, M., Deragon, J.-M., Bousquet-Antonelli, C., Lange, H., and, Gagliardi, D., (2013) Uridylation prevents 3′ trimming of oligoadenylated mRNAs. Nucleic Acids Res. 41, 7115-7127.
54. Shcherbik, N., Wang, M., Lapik, Y.R., Srivastava, L., and, Pestov, D.G., (2010) Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 11, 106-111.
55. Slevin, M.K., Meaux, S., Welch, J.D., Bigler, R., Miliani de Marval, P.L., Su, W., Rhoads, R.E., Prins, J.F., and, Marzluff, W.F., (2014) Deep sequencing shows multiple oligouridylations are required for 3′ to 5′ degradation of histone mRNAs on polyribosomes. Mol. Cell, 53, 1020-1030.
56. Sloan, K.E., Mattijssen, S., Lebaron, S., Tollervey, D., Pruijn, G.J.M., and, Watkins, N.J., (2013) Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol. 200, 577-588.
57. Staals, R.H.J., Bronkhorst, A.W., Schilders, G., Slomovic, S., Schuster, G., Heck, A.J.R., Raijmakers, R., and, Pruijn, G.J.M., (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J. 29, 2358-2367.
58. Tafforeau, L., Zorbas, C., Langhendries, J.-L., Mullineux, S.-T., Stamatopoulou, V., Mullier, R., Wacheul, L., and, Lafontaine, D.L.J., (2013) The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol. Cell, 51, 539-551.
59. Teng, T., Thomas, G., and, Mercer, C.A., (2013) Growth control and ribosomopathies. Curr. Opin. Genet. Dev. 23, 63-71.
60. Thomson, E., and, Tollervey, D., (2010) The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol. 30, 976-984.
61. Tomecki, R., Kristiansen, M.S., Lykke-Andersen, S., et al. (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J. 29, 2342-2357.
62. Torchet, C., and, Hermann-Le Denmat, S., (2000) Bypassing the rRNA processing endonucleolytic cleavage at site A2 in Saccharomyces cerevisiae. RNA, 6, 1498-1508.
63. Ustianenko, D., Hrossova, D., Potesil, D., Chalupnikova, K., Hrazdilova, K., Pachernik, J., Cetkovska, K., Uldrijan, S., Zdrahal, Z., and, Vanacova, S., (2013) Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA, 19, 1632-1638.
64. Vanacova, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G., and, Keller, W., (2005) A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189.
65. Vetter, G., Hily, J.-M., Klein, E., Schmidlin, L., Haas, M., Merkle, T., and, Gilmer, D., (2004) Nucleo-cytoplasmic shuttling of the beet necrotic yellow vein virus RNA-3-encoded p25 protein. J. Gen. Virol. 85, 2459-2469.
66. Weis, B.L., Palm, D., Missbach, S., Bohnsack, M.T., and, Schleiff, E., (2015) atBRX1-1 and atBRX1-2 are involved in an alternative rRNA processing pathway in Arabidopsis thaliana. RNA, 21, 415-425.
67. Wery, M., Ruidant, S., Schillewaert, S., Leporé, N., and, Lafontaine, D.L.J., (2009) The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA, 15, 406-419.
68. Wyers, F., Rougemaille, M., Badis, G., et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell, 121, 725-737.
69. Xi, L., Moscou, M.J., Meng, Y., Xu, W., Caldo, R.A., Shaver, M., Nettleton, D., and, Wise, R.P., (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.
70. Zakrzewska-Placzek, M., Souret, F.F., Sobczyk, G.J., Green, P.J., and, Kufel, J., (2010) Arabidopsis thaliana XRN2 is required for primary cleavage in the pre-ribosomal RNA. Nucleic Acids Res. 38, 4487-4502.
71. Zhang, W., Murphy, C., and, Sieburth, L.E., (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc. Natl Acad. Sci. 107, 15981-15985.
72. Zhao, Y., Yu, Y., Zhai, J., Ramachandran, V., Dinh, T.T., Meyers, B.C., Mo, B., and, Chen, X., (2012) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr. Biol. 22, 689-694.
73. Zimmer, S.L., Schein, A., Zipor, G., Stern, D.B., and, Schuster, G., (2009) Polyadenylation in Arabidopsis and Chlamydomonas organelles: the input of nucleotidyltransferases, poly(A) polymerases and polynucleotide phosphorylase. Plant J. 59, 88-99.