Translational landscape of photomorphogenic Arabidopsis

Plant Cell

Volumn 25, Issue 10, 2013, Pages 3699-3710

  Liu, Ming Jung ^a,d   Wu, Szu Hsien ^a,b,c   Wu, Jing Fen ^a   Lin, Wen Dar ^a   Wu, Yi Chen ^a   Tsai, Tsung Ying ^a   Tsai, Huang Lung ^a   Wu, Shu Hsing ^a,b,c  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

MESSENGER RNA; MICRORNA; PLANT RNA; START CODON;

ARABIDOPSIS; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; LIGHT; MORPHOGENESIS; OPEN READING FRAME; PROTEIN SYNTHESIS; RADIATION RESPONSE; RIBOSOME; SEQUENCE ANALYSIS; START CODON;

ARABIDOPSIS; CHROMOSOME MAPPING; CODON, INITIATOR; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; LIGHT; MICRORNAS; MORPHOGENESIS; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, PLANT; SEQUENCE ANALYSIS, RNA;

EID: 84888404338     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.114769     Document Type: Article

References (68)

1. Alatorre-Cobos, F., Cruz-Ramírez, A., Hayden, C.A., Pérez-Torres, C.A., Chauvin, A.L., Ibarra-Laclette, E., Alva-Cortés, E., Jorgensen, R.A., and Herrera-Estrella, L. (2012). Translational regulation of Arabidopsis XIPOTL1 is modulated by phosphocholine levels via the phylogenetically conserved upstream open reading frame 30. J. Exp. Bot. 63: 5203-5221.
2. Alexa, A., Rahnenführer, J., and Lengauer, T. (2006). Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607.
3. Arava, Y., Wang, Y., Storey, J.D., Liu, C.L., Brown, P.O., and Herschlag, D. (2003). Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100: 3889-3894.
4. Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
5. Bazzini, A.A., Lee, M.T., and Giraldez, A.J. (2012). Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336: 233-237.
6. Beauclair, L., Yu, A., and Bouché, N. (2010). MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J. 62: 454-462.
7. Branco-Price, C., Kaiser, K.A., Jang, C.J., Larive, C.K., and Bailey-Serres, J. (2008). Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56: 743-755.
8. Branco-Price, C., Kawaguchi, R., Ferreira, R.B., and Bailey-Serres, J. (2005). Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann. Bot. (Lond.) 96: 647-660.
9. Brar, G.A., Yassour, M., Friedman, N., Regev, A., Ingolia, N.T., and Weissman, J.S. (2012). High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335: 552-557.
10. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., and Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190.
11. Chang, C.S., Li, Y.H., Chen, L.T., Chen, W.C., Hsieh, W.P., Shin, J., Jane, W.N., Chou, S.J., Choi, G., Hu, J.M., Somerville, S., and Wu, S.H. (2008). LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J. 54: 205-219.
12. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022-2025.
13. Chen, X. (2010). Small RNAs-Secrets and surprises of the genome. Plant J. 61: 941-958.
14. Cunillera, N., Boronat, A., and Ferrer, A. (1997). The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 272: 15381-15388.
15. Djuranovic, S., Nahvi, A., and Green, R. (2012). MiRNA-mediated gene silencing by translational repression followed bymRNA deadenylation and decay. Science 336: 237-240.
16. Fabian, M.R., Sonenberg, N., and Filipowicz, W. (2010). Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79: 351-379.
17. Fritsch, C., Herrmann, A., Nothnagel, M., Szafranski, K., Huse, K., Schumann, F., Schreiber, S., Platzer, M., Krawczak, M., Hampe, J., and Brosch, M. (2012). Genome-wide search for novel human uORFs and N-terminal protein extensions using ribosomal footprinting. Genome Res. 22: 2208-2218.
18. Gandikota, M., Birkenbihl, R.P., Höhmann, S., Cardon, G.H., Saedler, H., and Huijser, P. (2007). The miRNA156/157 recognition element in the 39 UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 49: 683-693.
19. Guo, H., Ingolia, N.T., Weissman, J.S., and Bartel, D.P. (2010). Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
20. Hanfrey, C., Franceschetti, M., Mayer, M.J., Illingworth, C., and Michael, A.J. (2002). Abrogation of upstream open reading framemediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. J. Biol. Chem. 277: 44131-44139.
21. Hausser, J., Syed, A.P., Bilen, B., and Zavolan, M. (2013). Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res. 23: 604-615.
22. Hayden, C.A., and Jorgensen, R.A. (2007). Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes. BMC Biol. 5: 32.
23. Hood, H.M., Neafsey, D.E., Galagan, J., and Sachs, M.S. (2009). Evolutionary roles of upstream open reading frames in mediating gene regulation in fungi. Annu. Rev. Microbiol. 63: 385-409.
24. Huntzinger, E., and Izaurralde, E. (2011). Gene silencing by microRNAs: Contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12: 99-110.
25. Imai, A., Hanzawa, Y., Komura, M., Yamamoto, K.T., Komeda, Y., and Takahashi, T. (2006). The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133: 3575-3585.
26. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M., and Weissman, J.S. (2012). The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc. 7: 1534-1550.
27. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R., and Weissman, J.S. (2009). Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
28. Ingolia, N.T., Lareau, L.F., and Weissman, J.S. (2011). Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147: 789-802.
29. Jackson, R.J., Hellen, C.U., and Pestova, T.V. (2010). The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11: 113-127.
30. Juntawong, P., and Bailey-Serres, J. (2012). Dynamic light regulation of translation status in Arabidopsis thaliana. Front Plant Sci 3: 66.
31. Kawaguchi, R., Girke, T., Bray, E.A., and Bailey-Serres, J. (2004). Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J. 38: 823-839.
32. Kim, B.H., Cai, X., Vaughn, J.N., and von Arnim, A.G. (2007). On the functions of the h subunit of eukaryotic initiation factor 3 in late stages of translation initiation. Genome Biol. 8: R60.
33. Kozak, M. (1986). Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292.
34. Kozak, M. (1987a). An analysis of 59-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15: 8125-8148.
35. Kozak, M. (1987b). Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell. Biol. 7: 3438-3445.
36. Kozak, M. (2001). Constraints on reinitiation of translation in mammals. Nucleic Acids Res. 29: 5226-5232.
37. Lackner, D.H., and Bähler, J. (2008). Translational control of gene expression from transcripts to transcriptomes. Int. Rev. Cell Mol. Biol. 271: 199-251.
38. Lanet, E., Delannoy, E., Sormani, R., Floris, M., Brodersen, P., Crété, P., Voinnet, O., and Robaglia, C. (2009). Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21: 1762-1768.
39. Lee, S., Liu, B., Lee, S., Huang, S.X., Shen, B., and Qian, S.B. (2012). Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. USA 109: E2424-E2432.
40. Li, J.F., Chung, H.S., Niu, Y., Bush, J., McCormack, M., and Sheen, J. (2013a). Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell 25: 1507-1522.
41. Li, S., et al. (2013b). MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153: 562-574.
42. Lin, W.D., Chen, Y.C., Ho, J.M., and Hsiao, C.D. (2006). GOBU: Toward an integration interface for biological objects. J. Inf. Sci. Eng. 22: 19-29.
43. Liu, M.J., Wu, S.H., Chen, H.M., and Wu, S.H. (2012). Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis. Mol. Syst. Biol. 8: 566.
44. Mackenzie, S.A. (2005). Plant organellar protein targeting: A traffic plan still under construction. Trends Cell Biol. 15: 548-554.
45. Matsuura, H., Ishibashi, Y., Shinmyo, A., Kanaya, S., and Kato, K. (2010). Genome-wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana. Plant Cell Physiol. 51: 448-462.
46. Medenbach, J., Seiler, M., and Hentze, M.W. (2011). Translational control via protein-regulated upstream open reading frames. Cell 145: 902-913.
47. Meijer, H.A., and Thomas, A.A. (2003). Ribosomes stalling on uORF1 in the Xenopus Cx41 59 UTR inhibit downstream translation initiation. Nucleic Acids Res. 31: 3174-3184.
48. Melamed, D., and Arava, Y. (2007). Genome-wide analysis of mRNA polysomal profiles with spotted DNA microarrays. Methods Enzymol. 431: 177-201.
49. Morris, D.R., and Geballe, A.P. (2000). Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20: 8635-8642.
50. Mustroph, A., Juntawong, P., and Bailey-Serres, J. (2009). Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol. Biol. 553: 109-126.
51. Nakamura, Y., Gojobori, T., and Ikemura, T. (2000). Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res. 28: 292.
52. Nicolaï, M., Roncato, M.A., Canoy, A.S., Rouquié, D., Sarda, X., Freyssinet, G., and Robaglia, C. (2006). Large-scale analysis of mRNA translation states during sucrose starvation in Arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control. Plant Physiol. 141: 663-673.
53. Nishimura, T., Wada, T., Yamamoto, K.T., and Okada, K. (2005). The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17: 2940-2953.
54. Pesole, G., Gissi, C., Grillo, G., Licciulli, F., Liuni, S., and Saccone, C. (2000). Analysis of oligonucleotide AUG start codon context in eukariotic mRNAs. Gene 261: 85-91.
55. Piques, M., Schulze, W.X., Höhne, M., Usadel, B., Gibon, Y., Rohwer, J., and Stitt, M. (2009). Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol. Syst. Biol. 5: 314.
56. Rajkowitsch, L., Vilela, C., Berthelot, K., Ramirez, C.V., and McCarthy, J.E. (2004). Reinitiation and recycling are distinct processes occurring downstream of translation termination in yeast. J. Mol. Biol. 335: 71-85.
57. Ribeiro, D.M., Araújo, W.L., Fernie, A.R., Schippers, J.H., and Mueller-Roeber, B. (2012). Translatome and metabolome effects triggered by gibberellins during rosette growth in Arabidopsis. J. Exp. Bot. 63: 2769-2786.
58. Rodriguez Milla, M.A., Maurer, A., Rodriguez Huete, A., and Gustafson, J.P. (2003). Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J. 36: 602-615.
59. Rosado, A., Li, R., van de Ven, W., Hsu, E., and Raikhel, N.V. (2012). Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc. Natl. Acad. Sci. USA 109: 19537-19544.
60. Roy, B., Vaughn, J.N., Kim, B.H., Zhou, F., Gilchrist, M.A., and Von Arnim, A.G. (2010). The h subunit of eIF3 promotes reinitiation competence during translation of mRNAs harboring upstream open reading frames. RNA 16: 748-761.
61. Shu, P., Dai, H., Gao, W., and Goldman, E. (2006). Inhibition of translation by consecutive rare leucine codons in E. coli: Absence of effect of varying mRNA stability. Gene Expr. 13: 97-106.
62. Sormani, R., Delannoy, E., Lageix, S., Bitton, F., Lanet, E., Saez-Vasquez, J., Deragon, J.M., Renou, J.P., and Robaglia, C. (2011). Sublethal cadmium intoxication in Arabidopsis thaliana impacts translation at multiple levels. Plant Cell Physiol. 52: 436-447.
63. Stadler, M., Artiles, K., Pak, J., and Fire, A. (2012). Contributions of mRNA abundance, ribosome loading, and post-or peri-translational effects to temporal repression of C. elegans heterochronic miRNA targets. Genome Res. 22: 2418-2426.
64. Thatcher, L.F., Carrie, C., Andersson, C.R., Sivasithamparam, K., Whelan, J., and Singh, K.B. (2007). Differential gene expression and subcellular targeting of Arabidopsis glutathione S-transferase F8 is achieved through alternative transcription start sites. J. Biol. Chem. 282: 28915-28928.
65. Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I., and Pilpel, Y. (2010). An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141: 344-354.
66. Varenne, S., Buc, J., Lloubes, R., and Lazdunski, C. (1984). Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J. Mol. Biol. 180: 549-576.
67. Wiese, A., Elzinga, N., Wobbes, B., and Smeekens, S. (2004). A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16: 1717-1729.
68. Yang, L., Wu, G., and Poethig, R.S. (2012). Mutations in the GWrepeat protein SUO reveal a developmental function for microRNAmediated translational repression in Arabidopsis. Proc. Natl. Acad. Sci. USA 109: 315-320.