Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis

Molecular Systems Biology

Volumn 5, Issue , 2009, Pages

  Piques, Maria ^a   Schulze, Waltraud X ^a   Höhne, Melanie ^a   Usadel, Björn ^a   Gibon, Yves ^a,b   Rohwer, Johann ^a,c   Stitt, Mark ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Arabidopsis; Polysomes; Quantitative RT PCR; Ribosome; Translation

Indexed keywords

ENZYME; ARABIDOPSIS PROTEIN; MESSENGER RNA;

ARABIDOPSIS; ARTICLE; BIODEGRADATION; BREATHING; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME SYNTHESIS; GENE NUMBER; GENETIC TRANSCRIPTION; MOLECULAR DYNAMICS; NONHUMAN; PLANT GROWTH; POLYSOME; PRIORITY JOURNAL; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; ROSETTE FORMATION; TRANSLATION INITIATION; BIOSYNTHESIS; CELL FRACTIONATION; CIRCADIAN RHYTHM; CODON; DARKNESS; ENZYMOLOGY; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT LEAF; PROTEIN SYNTHESIS;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CIRCADIAN RHYTHM; CODON; DARKNESS; GENE DOSAGE; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SUBCELLULAR FRACTIONS;

EID: 73149106617     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2009.68     Document Type: Article

References (82)

1. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100: 3889-3894
2. Bassham DC (2007) Plant autophagy-more than a starvation response. Curr Opinion Plant Biol 10: 587-593
3. Beilharz TH, Preiss T (2004) Translational profiling: the genome-wide measure of the nascent proteome. Brief Funct Genomic Proteomic 3: 103-111
4. Beilharz TH, Preiss T (2007) Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome. RNA 13: 982-997
5. Beyer A, Hollunder J, Nasheuer H-P, Wilhelm T (2004) Posttranscriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale. Mol Cell Proteomics 3: 1083-1092
6. Bläsing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257-3281
7. Brandt F, Etchells SA, Ortiz JO, Elcock AH, Hartl FU, Baumeister W (2009) The native 3D organization of bacterial polysomes. Cell 136: 261-271 BRENDA. The Comprehensive Enzyme Information System (http://www.brenda-enzymes.info/)
8. Brockmann R, Beyer A, Heinisch JJ, Wilhelm T (2007) Posttranscriptional expression regulation: what determines translation rates? PLoS Comp Biol 3: 0531-0539
9. Burrell MM, Mooney PJ, Blundy M, Carter D, Wilson F, Green J, Blundy KS, Aprees T (1994) Genetic manipulation of 6-phosphofructokinase in potato-tubers. Planta 194: 95-101
10. Chiapello H, Lisacek F, Caboche M, Henaut A (1998) Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 209: GC1-GC38
11. CoreTeam RD (2008) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing
12. Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbonlimited conditions. Plant Physiol 142: 1574-1588
13. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17
14. Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proc Natl Acad Sci USA 96: 4482-4487
15. Dyer TA, Miller RH, Greenwood AD (1971) Leaf nucleic acids: I. Characteristics and role in the differentiation of plastids. J Exp Bot 22: 125-136
16. Ernst D, Apfelbock A, Bergmann A, Weyrauch C (1990) Rhythmic regulation of the light-harvesting chlorophyll a/b protein and the small subunit of ribulose-1,5-bisphosphate carboxylase mRNA in rye seedlings. Photochem Photobiol 52: 22-33
17. Esquivel MG, Ferreira RB, Teixeira AR (1998) Protein degradation in C- 3 and C-4 plants with particular reference to ribulose bisphosphate carboxylase and glycolate oxidase. J Exp Bot 49: 807-816
18. Farquhar GD, von Caemmerer S, Berry JA (2001) Models of photosynthesis. Plant Physiol 125: 42-45
19. Foyer CH, Ferrario-Mery S, Huber SC (2000) Regulation of carbon fluxes in the cytosol: coordination of sucrose synthesis, nitrate reduction and organic acid and amino acid biosynthesis. In Photosynthesis: Physiology and metabolism, Leegood RC, Sharkey TD, von Caemmerer S (eds), pp 177-203. Dordrecht, Netherlands: Kluwer Academic Publishers
20. Fritz C, Mueller C, Matt P, Feil R, Stitt M (2006) Impact of the C-N status on the amino acid profile in tobacco source leaves. Plant Cell Environ 29: 2055-2076
21. Geiger DR, Servaites JC, Fuchs MA (2000) Role of starch in carbon translocation and partitioning at the plant level. Funct Plant Biol 27: 571-582
22. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JHM, Palacios N, Cross J, Selbig J, Stitt M (2004b) 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 16: 3304-3325
23. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004a) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADPglucose pyrophosphorylase in the following light period. Plant J 39: 847-862 (Pubitemid 39320558)
24. Gibon Y, Pyl E-T, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32: 859-874
25. Gibon Y, Usadel B, Blaesing O, Kamlage B, Hoehne M, Trethewey R, Stitt M (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7: R76
26. Hachiya T, Terashima I, Noguchi K (2007) Increase in respiratory cost at high growth temperature is attributed to high protein turnover cost in Petunia-hybrida petals. Plant Cell Environ 30: 1269-1283
27. Hannemann J, Poorter H, Usadel B, Bläsing OE, Finck A, Tardieu F, Atkin OK, Pons T, Stitt M, Gibon Y (2009) Xeml Lab: a tool that supports the design of experiments at a graphical interface and generates computer-readable meta-data files, which capture information about genotypes, growth conditions, environmental perturbations and sampling strategy. Plant Cell Environ 32: 1185-1200
28. Huege J, Sulpice R, Gibon Y, Lisec J, Koehl K, Kopka J (2007) GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after (CO2)-C-13 labelling. Phytochem Rev 68: 2258-2272
29. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272
30. Jenner HL, Winning BM, Millar AH, Tomlinson KL, Leaver CJ, Hill SA (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126: 1139-1149
31. Jones E, Oilphant T, Peterson P (2001) SciPy: open source scientific tools for Python. http://www.scipy.org
32. Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52: 1981-1989
33. Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 33: 955-965
34. Kawaguchi R, Girke T, Bray EA, 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
35. Kawaguchi R, Williams AJ, Bray EA, Bailey-Serres J (2003) Waterdeficit- induced translational control in Nicotiana tabacum. Plant Cell Environ 26: 221-229
36. Keurentjes J, Sulpice R, Gibon Y, Steinhauser M-C, Fu J, Koornneef M, Stitt M, Vreugdenhil D (2008) Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biol 9: R129
37. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, Schubert F, Preiss T, Bahler J (2007) A network of multiple regulatory layers shapes gene expression in fission yeast. Mol Cell 26: 145-155
38. Lea US, Tem Hoopen F, Provan F, Kaiser WM, Meyer C, Lillo C (2004) Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue. Planta 219: 59-65
39. Lillo C (2008) Signalling cascades integrating light-enhanced nitrate metabolism. Biochem J 415: 11-19
40. Lodish HF, Jacobsen M (1972) Regulation of hemoglobin synthesis. Equal rates of translation and termination of a- and b-globin chains. J Biol Chem 247: 3622-3629
41. MacKay VL, Li X, Flory MR, Turcott E, Law GL, Serikawa KA, Xu XL, Lee H, Goodlett DR, Aebersold R, Zhao LP, Morris DR (2004) Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteomics 3: 478-489
42. Manjunath S, Lee CH, VanWinkle P, Bailey-Serres J (1998) Molecular and biochemical characterization of cytosolic phosphoglucomutase in maize. Expression during development and in response to oxygen deprivation. Plant Physiol 117: 997-1006
43. Marín-Navarro J, Manuell A, Wu J, P Mayfield S (2007) Chloroplast translation regulation. Photosynthesis Res 94: 359-374
44. Mathews MB, Sonenberg N, Hershey JWB (2007) Origins and principles of translational control. In Translational Control in Biology and Medicine, Mathews MB, Sonenberg N, Hershey JWB (eds), pp 1-40. New York, USA: Cold Spring Harbor laboratory press
45. Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001) Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ 24: 1119-1137 NCBI. The National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/blast)
46. Noguchi K, Nakajima N, Terashima I (2001) Acclimation of leaf respiratory properties in Alocasia odora following reciprocal transfers of plants between high- and low-light environments. Plant Cell Environ 24: 831-839
47. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50: 1093-1106
48. Olsen JV, Ong S-E, Mann M (2004) Trypsin cleaves exclusively c-terminal to arginine and lysine residues.Mol Cell Proteomics 3: 608-614
49. Pace DA, Manahan DT (2007) Cost of protein synthesis and energy allocation during development of Antarctic sea urchin embryos and larvae. Biol Bull 212: 115-129
50. Palmiter DR (1974) Differential rates of initiation on conalbumin and ovalbumin messenger ribonucleic acid in reticulocyte lysates. J Biol Chem 249: 6779-6787
51. Penning de Vries FWT (1975) The cost of maintenance processes in plant cells. Ann Bot 39: 77-92
52. Perry RP (2007) Balanced production of ribosomal proteins. Gene 401: 1-3
53. Proud CG (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403: 217-234
54. Puigbo P, Bravo IG, Garcia-Vallve S (2008) E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI). BMC Bioinformatics 9: 65
55. Qin X, Ahn S, Speed T, Rubin G (2007) Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol 8: R63
56. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66
57. Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trend Genet 16: 276-277
58. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53: 102-110
59. Rodermel S, Haley J, Jiang C-Z, Tsai C-H, Bogorad L (1996) Amechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proc Natl Acad Sci USA 93: 3881-3885
60. Ryazanov AG, Rudkin BB, Spirin AS (1991) Regulation of protein synthesis at the elongation stage: new insights into the control of gene expression in eukaryotes. FEBS Lett 285: 170-175
61. Scheibe R, Stitt M (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol Biochem 26: 473-481
62. Scheible W-R, González-Fontes A, Morcuende R, Lauerer M, Geiger M, Glaab J, Gojon A, Schulze E-D, Stitt M (1997) Tobacco mutants with a decreased number of functional nia genes compensate by modifying the diurnal regulation of transcription, post-translational modification and turnover of nitrate reductase. Planta 203: 304-319
63. Serina L, Blondin C, Krin E, Sismeiro O, Danchin A, Sakamoto H, Gilles AM, Barzu O (1995) Escherichia coli Ump-kinase, a member of the aspartokinase family, is a hexamer regulated by guaninenucleotides and UTP. Biochemistry (Mosc) 34: 5066-5074
64. Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24: 28-38
65. Simpson E, Cooke RJ, Davies DD (1981) Measurement of protein degradation in leaves of Zea mays using [3H]acetic anhydride and tritiated water. Plant Physiol 67: 1214-1219
66. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149
67. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136: 2687-2699
68. Steinhauser D, Usadel B, Lüdemann A, Thimm O, Kopka J (2004) CSBDB: Acomprehensive systems biology database. Bioinformatics 20: 3647-3651
69. Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. Funct Plant Biol 34: 526-549
70. Sulpice R, Tschoep H, von Korff M, Bussis D, Usadel B, Hohne M, Witucka-Wall H, Altmann T, Stitt M, Gibon Y (2007) Description and applications of a rapid and sensitive non-radioactivemicroplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Cell Environ 30: 1163-1175 TAIR. The Arabidopsis Information Resource (http://www. arabidopsis.org/)
71. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939
72. Tschoep H, Gibon Y, Carillo P, Armengaud P, Szecowka M, Nunes-Nesi A, Fernie AR, Koehl K, Stitt M (2009) Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. Plant Cell Environ 32: 300-318
73. Usadel B, Blasing OE, Gibon Y, Retzlaff K, Hohne M, Gunther M, StittM (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146: 1834-1861
74. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10: 385-397
75. von Ahlfen S, Missel A, Bendrat K, Schlumpberger M (2007) Determinants of RNA quality from FFPE samples. PLoS ONE 2: e1261
76. Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440
77. Weiner H, Kaiser WM (1999) 14-3-3 proteins control proteolysis of nitrate reductase in spinach leaves. FEBS Lett 455: 75-78
78. Wolin SL, Walter P (1988) Ribosome pausing and stacking during translation of a eukaryotic messenger-RNA. EMBO J 7: 3559-3569
79. Wostrikoff K, Stern D (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc. Natl Acad Sci USA 104: 6466-6471
80. Wright F (1990) The effective number of codons used in a gene. Gene 87: 23-29
81. Wright SI, Yau CBK, Loosely M, Meyers BC (2004) Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol Biol Evol 21: 1719-1726
82. Zhu X-G, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145: 513-526