Increased sucrose levels mediate selective mRNA translation in Arabidopsis

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Gamm, Magdalena ^a   Peviani, Alessia ^a   Honsel, Anne ^b   Snel, Berend ^a   Smeekens, Sjef ^a   Hanson, Johannes ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Arabidopsis; Protein synthesis; Sugar signaling; Translational regulation

Indexed keywords

ARABIDOPSIS PROTEIN; RIBOSOME PROTEIN; SUCROSE;

ARABIDOPSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; POLYSOME; PROTEIN SYNTHESIS; RADIATION RESPONSE; RIBOSOME; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LIGHT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; SEEDLINGS; SIGNAL TRANSDUCTION; SUCROSE;

EID: 84988711001     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0306-3     Document Type: Article

References (68)

1. Pal SK, Liput M, Piques M, Ishihara H, Obata T, Martins MCM, Sulpice R, van Dongen JT, Fernie AR, Yadav UP, Lunn JE, Usadel B, Stitt M: Diurnal changes of polysome loading track sucrose content in the rosette of wild-type arabidopsis and the starchless pgm mutant. Plant Physiol 2013, 162:1246-1265.
2. Stitt M: Progress in understanding and engineering primary plant metabolism. Curr Opin Biotechnol 2012, 24:229-238.
3. Kapp LD, Lorsch JR: The molecular mechanics of eukaryotic translation. Annu Rev Biochem 2004, 73:657-704.
4. Ma XM, Blenis J: Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009, 10:307-318.
5. Jackson RJ, Hellen CUT, Pestova TV: The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010, 11:113-127.
6. Kawaguchi R, Bailey-Serres J: Regulation of translational initiation in plants. Curr Opin Plant Biol 2002, 5:460-465.
7. Esposito AM, Mateyak M, He D, Lewis M, Sasikumar AN, Hutton J, Copeland PR, Kinzy TG: Eukaryotic polyribosome profile analysis. J Vis Exp 2010, 40:e1948.
8. Kawaguchi R, Girke T, Bray E A, Bailey-Serres J: Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 2004, 38:823-839.
9. Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J: Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 2005, 96:647-660.
10. Branco-Price C, Kaiser K A, Jang CJH, Larive CK, Bailey-Serres J: Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 2008, 56:743-755.
11. Matsuura H, Ishibashi Y, Shinmyo A, Kanaya S, Kato K: Genome-wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana. Plant Cell Physiol 2010, 51:448-462.
12. Ueda K, Matsuura H, Yamaguchi M, Demura T, Kato K: Genome-wide analyses of changes in translation state caused by elevated temperature in Oryza sativa. Plant Cell Physiol 2012, 53:1481-1491.
13. Bailey-Serres J, Sorenson R, Juntawong P: Getting the message across: cytoplasmic ribonucleoprotein complexes. Trends Plant Sci 2009, 14:443-453.
14. Roy B, von Arnim AG: Translational regulation of cytoplasmic mRNAs. Arab B 2013, 11:e0165.
15. Juntawong P, Girke T, Bazin J, Bailey-Serres J: Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis. Proc Natl Acad Sci U S A 2014, 111:E203-E212.
16. Sorenson R, Bailey-Serres J: Selective mRNA sequestration by OLIGOURIDYLATE-BINDING PROTEIN 1 contributes to translational control during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A 2014, 111:2373-2378.
17. Nicolaï M, Roncato MA, Canoy AS, Rouquié D, Sarda X, Freyssinet G, Robaglia C: 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 2006, 141:663-673.
18. Piques M, Schulze WX, Höhne M, Usadel B, Gibon Y, Rohwer J, Stitt M: Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol Syst Biol 2009, 5:314.
19. Juntawong P, Bailey-Serres J: Dynamic light regulation of translation status in Arabidopsis thaliana. Front Plant Sci 2012, 3:66.
20. Jiménez-López S, Mancera-Martínez E, Donayre-Torres A, Rangel C, Uribe L, March S, Jiménez-Sánchez G, Sánchez de Jiménez E: Expression profile of maize (Zea mays L.) embryonic axes during germination: translational regulation of ribosomal protein mRNAs. Plant Cell Physiol 2011, 52:1719-1733.
21. Tiruneh BS, Kim B-H, Gallie DR, Roy B, von Arnim AG: The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant. BMC Biol 2013, 11:123.
22. Barakat A, Szick-Miranda K, Chang I-F, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J: The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome 1. Plant Physiol 2001, 127:398-415.
23. Carroll AJ, Heazlewood JL, Ito J, Millar AH: Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteomics 2008, 7:347-369.
24. Chang I, Szick-Miranda K, Pan S, Bailey-Serres J: Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes. Plant Physiol 2005, 137(March):848-862.
25. Giavalisco P, Wilson D, Kreitler T, Lehrach H, Klose J, Gobom J, Fucini P: High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol Biol 2005, 57:577-591.
26. Mcintosh KB, Bonham-Smith PC: Ribosomal protein gene regulation: what about plants? Can J Bot 2006, 362:342-362.
27. Degenhardt RF, Bonham-Smith PC: Transcript profiling demonstrates absence of dosage compensation in Arabidopsis following loss of a single RPL23a paralog. Planta 2008, 228:627-640.
28. Schippers JHM, Mueller-Roeber B: Ribosomal composition and control of leaf development. Plant Sci 2010, 179:307-315.
29. Byrne ME: A role for the ribosome in development. Trends Plant Sci 2009, 14:512-519.
30. Xue S, Barna M: Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 2012, 13:355-369.
31. Hummel M, Cordewener JHG, de Groot JCM, Smeekens S, America AHP, Hanson J: Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics. Proteomics 2012, 12:1024-1038.
32. Turkina MV, Klang Årstrand H, Vener AV: Differential phosphorylation of ribosomal proteins in Arabidopsis thaliana plants during day and night. PLoS ONE 2011, 6:e29307.
33. Boex-Fontvieille E, Daventure M, Jossier M, Zivy M, Hodges M, Tcherkez G: Photosynthetic control of Arabidopsis leaf cytoplasmic translation initiation by protein phosphorylation. PLoS ONE 2013, 8:e70692.
34. Liu M-J, Wu S-H, Chen H-M, Wu S-H: Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis. Mol Syst Biol 2012, 8:566.
35. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Ho M, Palacios N, Cross J, Selbig J, Stitt M: A robot-based platform to measure multiple enzyme activities in arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 2004, 16(December):3304-3325.
36. Yi X, Du Z, Su Z: PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Res 2013, 41:W98-W103.
37. Gonzali S, Loreti E, Solfanelli C, Novi G, Alpi A, Perata P: Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis. J Plant Res 2006, 119:115-123.
38. Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M: Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 2008, 146:1834-1861.
39. Baena-González E, Rolland F, Thevelein JM, Sheen J: A central integrator of transcription networks in plant stress and energy signalling. Nature 2007, 448:938-942.
40. Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S: Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol 2005, 138(June):1027-1036.
41. Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S, Kim S-Y, Stacey MG, Stacey G: A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008, 20:471-481.
42. Robaglia C, Thomas M, Meyer C: Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 2012, 15:301-307.
43. Xiong Y, Sheen J: TOR Signaling Networks in Plant Growth and Metabolism. Plant Physiol 2014, 164:499-512.
44. Rolland F, Baena-Gonzalez E, Sheen J: Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 2006, 57:675-709.
45. Koch KE: Carbohydrate-Modulated Gene Expression in Plants. Annu Rev Plant Physiol Plant Mol Biol 1996, 47:509-540.
46. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible W-R, Stitt M: Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 2007, 49:463-491.
47. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM: A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012, 485:109-113.
48. Deprost D, Truong H-N, Robaglia C, Meyer C: An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem Biophys Res Commun 2005, 326:844-850.
49. Ren M, Qiu S, Venglat P, Xiang D, Feng L, Selvaraj G, Datla R: Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 2011, 155:1367-1382.
50. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J: Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 2013, 496:181-186.
51. Schepetilnikov M, Dimitrova M, Mancera-Martínez E, Geldreich A, Keller M, Ryabova L: TOR and S6K1 promote translation reinitiation of uORFcontaining mRNAs via phosphorylation of eIF3h. EMBO J 2013, 32:1087-1102.
52. Perry RP: Balanced production of ribosomal proteins. Gene 2007, 401:1-3.
53. Liu M-J, Wu S-H, Wu J-F, Lin W-D, Wu Y-C, Tsai T-Y, Tsai H-L, Wu S-H: Translational landscape of photomorphogenic Arabidopsis. Plant Cell 2013, 25:3699-3710.
54. Ingolia NT: Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet 2014, 15:205-213.
55. Kawaguchi R, Bailey-Serres J: mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 2005, 33:955-965.
56. Vaughn JN, Ellingson SR, Mignone F, von Arnim A: Known and novel posttranscriptional regulatory sequences are conserved across plant families. RNA 2012, 18:368-384.
57. Gullberg J, Jonsson P, Nordström A, Sjöström M, Moritz T: Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal Biochem 2004, 331:283-295.
58. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, Fernie AR, Kopka J: GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 2005, 579:1332-1337.
59. Jonsson P, Johansson AI, Gullberg J, Trygg J, a J, Grung B, Marklund S, Sjöström M, Antti H, Moritz T: High-throughput data analysis for detecting and identifying differences between samples in GC/MS-based metabolomic analyses. Anal Chem 2005, 77:5635-5642.
60. Mustroph A, Juntawong P, Bailey-Serres J: Isolation of Plant Polysomal mRNA by Differential Centrifugation and Ribosome Immunopurification Methods. In Plant Syst Biol. Volume 553. Edited by Belostotsky DA. Totowa, NJ: Humana Press; 2009:109-126 [Methods in Molecular Biology™].
61. Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 1995, 57:289-300.
62. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
63. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
64. R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/
65. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman a FM: Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 2009, 37:e45.
66. Bailey TL, Boden M, Buske F A, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS: MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208.
67. Sun X, Yang Q, Xia X: An improved implementation of effective number of codons (Nc). Mol Biol Evol 2012, 30:191-196.
68. Von Arnim AG, Jia Q, Vaughn JN: Regulation of plant translation by upstream open reading frames. Plant Sci 2014, 214:1-12.