LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development

Plant Cell

Volumn 24, Issue 12, 2013, Pages 4930-4947

  Perea Resa, Carlos ^a   Hernández Verdeja, Tamara ^a,b   López Cobollo, Rosa ^a,c   Castellano, María del Mar ^a,b   Salinas, Julio ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873049075     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.103697     Document Type: Article

References (64)

1. Anderson, J.S.J., and Parker, R.P. (1998). The 39 to 59 degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 39 to 59 exonucleases of the exosome complex. EMBO J. 17: 1497-1506.
2. Barta, A., Kalyna, M., and Lorkovic, Z.J. (2008). Plant SR proteins and their functions. Curr. Top. Microbiol. Immunol. 326: 83-102.
3. Beelman, C.A., Stevens, A., Caponigro, G., LaGrandeur, T.E., Hatfield, L., Fortner, D.M., and Parker, R. (1996). An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 382: 642-646.
4. Beggs, J.D. (2005). Lsm proteins and RNA processing. Biochem. Soc. Trans. 33: 433-438.
5. Belostotsky, D.A., and Sieburth, L.E. (2009). Kill the messenger: mRNA decay and plant development. Curr. Opin. Plant Biol. 12: 96-102.
6. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., and Filipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124.
7. Bonnerot, C., Boeck, R., and Lapeyre, B. (2000). The two proteins Pat1p (Mrt1p) and Spb8p interact in vivo, are required for mRNA decay, and are functionally linked to Pab1p. Mol. Cell. Biol. 20: 5939-5946.
8. Bouveret, E., Rigaut, G., Shevchenko, A., Wilm, M., and Séraphin, B. (2000). A Sm-like protein complex that participates in mRNA degradation. EMBO J. 19: 1661-1671.
9. Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
10. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
11. Coller, J., and Parker, R. (2005). General translational repression by activators of mRNA decapping. Cell 122: 875-886.
12. Coller, J.M., Tucker, M., Sheth, U., Valencia-Sanchez, M.A., and Parker, R. (2001). The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 7: 1717-1727.
13. Cougot, N., Babajko, S., and Séraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165: 31-40.
14. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
15. Decker, C.J., Teixeira, D., and Parker, R. (2007). Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 179: 437-449.
16. Deng, X., Gu, L., Liu, C., Lu, T., Lu, F., Lu, Z., Cui, P., Pei, Y., Wang, B., Hu, S., and Cao, X. (2010). Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper premRNA splicing. Proc. Natl. Acad. Sci. USA 107: 19114-19119.
17. Dunckley, T., and 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.
18. English, J., Davenport, G., Elmayan, T., Vaucheret, H., and Baulcombe, D. (1997). Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J. 12: 597-603.
19. Furumizu, C., Tsukaya, H., and Komeda, Y. (2010). Characterization of EMU, the Arabidopsis homolog of the yeast THO complex member HPR1. RNA 16: 1809-1817.
20. Goda, H., et al. (2008). The AtGenExpress hormone and chemical treatment data set: Experimental design, data evaluation, model data analysis and data access. Plant J. 55: 526-542.
21. Goeres, D.C., Van Norman, J.M., Zhang, W., Fauver, N.A., Spencer, M.L., and Sieburth, L.E. (2007). Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell 19: 1549-1564.
22. Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D.S. (2012). Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 40(Database issue): D1178-D1186.
23. Gutiérrez, R.A., Ewing, R.M., Cherry, J.M., and Green, P.J. (2002). Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: Rapid decay is associated with a group of touchand specific clock-controlled genes. Proc. Natl. Acad. Sci. USA 99: 11513-11518.
24. Halbeisen, R.E., Galgano, A., Scherrer, T., and Gerber, A.P. (2008). Post-transcriptional gene regulation: From genome-wide studies to principles. Cell. Mol. Life Sci. 65: 798-813.
25. Hu, C.D., Chinenov, Y., and Kerppola, T.K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9: 789-798.
26. Ingelfinger, D., Arndt-Jovin, D.J., Lührmann, R., and Achsel, T. (2002). The human LSm1-7 proteins colocalize with the mRNAdegrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8: 1489-1501.
27. Kastenmayer, J.P., and Green, P.J. (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.
28. Kim, W.Y., Jung, H.J., Kwak, K.J., Kim, M.K., Oh, S.H., Han, Y.S., and Kang, H. (2010). The Arabidopsis U12-type spliceosomal protein U11/U12-31K is involved in U12 intron splicing via RNA chaperone activity and affects plant development. Plant Cell 22: 3951-3962.
29. Lange, H., and Gagliardi, D. (2010). The exosome and 39-59 RNA degradation in plants. Adv. Exp. Med. Biol. 702: 50-62.
30. Laubinger, S., Zeller, G., Henz, S.R., Sachsenberg, T., Widmer, C.K., Naouar, N., Vuylsteke, M., Schölkopf, B., Rätsch, G., and Weigel, D. (2008). At-TAX: A whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol. 9: R112.
31. Lee, B.H., Kapoor, A., Zhu, J., and Zhu, J.K. (2006). STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18: 1736-1749.
32. Lorkovic, Z.J. (2009). Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci. 14: 229-236.
33. Lorkovic, Z.J., Wieczorek Kirk, D.A., Lambermon, M.H., and Filipowicz, W. (2000). Pre-mRNA splicing in higher plants. Trends Plant Sci. 5: 160-167.
34. Matlin, A.J., Clark, F., and Smith, C.W. (2005). Understanding alternative splicing: Towards a cellular code. Nat. Rev. Mol. Cell Biol. 6: 386-398.
35. Medina, J., Catalá, R., and Salinas, J. (2001). Developmental and stress regulation of RCI2A and RCI2B, two cold-inducible genes of Arabidopsis encoding highly conserved hydrophobic proteins. Plant Physiol. 125: 1655-1666.
36. Meyer, S., Temme, C., and Wahle, E. (2004). Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39: 197-216.
37. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41.
38. Ner-Gaon, H., and Fluhr, R. (2006). Whole-genome microarray in Arabidopsis facilitates global analysis of retained introns. DNA Res. 13: 111-121.
39. Parker, R., and Song, H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
40. Pomeranz, M., Lin, P.C., Finer, J., and Jang, J.C. (2010). AtTZF gene family localizes to cytoplasmic foci. Plant Signal. Behav. 5: 190-192.
41. Proost, S., Van Bel, M., Sterck, L., Billiau, K., Van Parys, T., Van de Peer, Y., and Vandepoele, K. (2009). PLAZA: A comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21: 3718-3731.
42. Raab, S., and Hoth, S. (2007). A mutation in the AtPRP4 splicing factor gene suppresses seed development in Arabidopsis. Plant Biol. (Stuttg.) 9: 447-452.
43. Reddy, A.S. (2001). Nuclear pre-mRNA splicing in plants. Crit. Rev. Plant Sci. 20: 523-571.
44. Reijns, M.A., Alexander, R.D., Spiller, M.P., and Beggs, J.D. (2008). A role for Q/N-rich aggregation-prone regions in P-body localization. J. Cell Sci. 121: 2463-2472.
45. Rymarquis, L.A., Souret, F.F., and Green, P.J. (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.
46. Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805-808.
47. Sheth, U., and Parker, R. (2006). Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125: 1095-1109.
48. Souret, F.F., Kastenmayer, J.P., and Green, P.J. (2004). AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 15: 173-183.
49. Stauffer, E., Westermann, A., Wagner, G., and Wachter, A. (2010). Polypyrimidine tract-binding protein homologues from Arabidopsis underlie regulatory circuits based on alternative splicing and downstream control. Plant J. 64: 243-255.
50. Syed, N.H., Kalyna, M., Marquez, Y., Barta, A., and Brown, J.W. (2012). Alternative splicing in plants-Coming of age. Trends Plant Sci. 17: 616-623.
51. Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., and Parker, R. (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11: 371-382.
52. Tharun, S. (2009). Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell Mol. Biol. 272: 149-189.
53. Tharun, S., He, W., Mayes, A.E., Lennertz, P., Beggs, J.D., and Parker, R. (2000). Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404: 515-518.
54. Tharun, S., Muhlrad, D., Chowdhury, A., and Parker, R. (2005). Mutations in the Saccharomyces cerevisiae LSM1 gene that affect mRNA decapping and 39 end protection. Genetics 170: 33-46.
55. Unterholzner, L., and Izaurralde, E. (2004). SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16: 587-596.
56. Wahl, M.C., Will, C.L., and Lührmann, R. (2009). The spliceosome: Design principles of a dynamic RNP machine. Cell 136: 701-718.
57. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
58. Wang, B.B., and Brendel, V. (2004). The ASRG database: Identification and survey of Arabidopsis thaliana genes involved in premRNA splicing. Genome Biol. 5: R102.
59. Weber, C., Nover, L., and Fauth, M. (2008). Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J. 56: 517-530.
60. Xiong, L., Gong, Z., Rock, C.D., Subramanian, S., Guo, Y., Xu, W., Galbraith, D., and Zhu, J.K. (2001). Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev. Cell 1: 771-781.
61. Xu, J., and Chua, N.H. (2009). Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell 21: 3270-3279.
62. Xu, J., and Chua, N.H. (2011). Processing bodies and plant development. Curr. Opin. Plant Biol. 14: 88-93.
63. Xu, J., Yang, J.Y., Niu, Q.W., and Chua, N.H. (2006). Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18: 3386-3398.
64. Zhang, Z., et al. (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.