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PMID: 19888209 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Molecular systems biology ·Vol. 5 ·2009-00-00 ·Pages 314

Piques M, Schulze WX, Höhne M, Usadel B, Gibon Y, Rohwer J, Stitt M

Abstract

Plants are exposed to continual changes in the environment. The daily alternation between light and darkness results in massive recurring changes in the carbon budget, and leads to widespread changes in transcript levels. These diurnal changes are superimposed on slower changes in the environment. Quantitative molecular information about the numbers of ribosomes, of transcripts for 35 enzymes in central metabolism and their loading into polysomes is used to estimate translation rates in Arabidopsis rosettes, and explore the consequences for important sub-processes in plant growth. Translation rates for individual enzyme are compared with their abundance in the rosette to predict which enzymes are subject to rapid turnover every day, and which are synthesized at rates that would allow only slow adjustments to sustained changes of the environment, or resemble those needed to support the observed rate of growth. Global translation rates are used to estimate the energy costs of protein synthesis and relate them to the plant carbon budget, in particular the rates of starch degradation and respiration at night.

MeSH Terms
Arabidopsis/enzymology,genetics,growth & development Arabidopsis Proteins/biosynthesis,genetics Circadian Rhythm/genetics Codon/genetics Darkness Gene Dosage/genetics Gene Expression Regulation, Plant Plant Leaves/enzymology,genetics Polyribosomes/metabolism Protein Biosynthesis RNA, Messenger/genetics,metabolism Subcellular Fractions/metabolism
Chemicals
Arabidopsis Proteins Codon RNA, Messenger
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Piques Maria
Max Planck Institute of Molecular Plant Physiology, Am Muehlenberg 1, Potsdam-Golm, Germany.
Schulze Waltraud X
Höhne Melanie
Usadel Björn
Gibon Yves
Rohwer Johann
Stitt Mark
References (68)
68 references, click to expand
  1. Signalling to translation: how signal transduction pathways control the protein synthetic machinery.
    Biochem J. 2007 Apr 15;403(2):217-34 PMID: 17376031
  2. Posttranscriptional expression regulation: what determines translation rates?
    PLoS Comput Biol. 2007 Mar 23;3(3):e57 PMID: 17381238
  3. Impact of the C-N status on the amino acid profile in tobacco source leaves.
    Plant Cell Environ. 2006 Nov;29(11):2055-76 PMID: 17081241
  4. Signalling cascades integrating light-enhanced nitrate metabolism.
    Biochem J. 2008 Oct 1;415(1):11-9 PMID: 18778247
  5. 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 Dec;16(12):3304-25 PMID: 15548738
  6. 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. 1990 Jul;52(1):29-33 PMID: 2204946
  7. 14-3-3 proteins control proteolysis of nitrate reductase in spinach leaves.
    FEBS Lett. 1999 Jul 16;455(1-2):75-8 PMID: 10428475
  8. Trypsin cleaves exclusively C-terminal to arginine and lysine residues.
    Mol Cell Proteomics. 2004 Jun;3(6):608-14 PMID: 15034119
  9. Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale.
    Mol Cell Proteomics. 2004 Nov;3(11):1083-92 PMID: 15326222
  10. Plant autophagy--more than a starvation response.
    Curr Opin Plant Biol. 2007 Dec;10(6):587-93 PMID: 17702643
  11. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482-7 PMID: 10200288
  12. Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue.
    Planta. 2004 May;219(1):59-65 PMID: 14767769
  13. Differential rates of initiation of conalbumin and ovalbumin messenger ribonucleic acid in reticulocyte lysates.
    J Biol Chem. 1974 Nov 10;249(21):6779-87 PMID: 4420185
  14. The native 3D organization of bacterial polysomes.
    Cell. 2009 Jan 23;136(2):261-71 PMID: 19167328
  15. Models of photosynthesis.
    Plant Physiol. 2001 Jan;125(1):42-5 PMID: 11154292
  16. EMBOSS: the European Molecular Biology Open Software Suite.
    Trends Genet. 2000 Jun;16(6):276-7 PMID: 10827456
  17. Coordination of carbon supply and plant growth.
    Plant Cell Environ. 2007 Sep;30(9):1126-49 PMID: 17661751
  18. Xeml Lab: a tool that supports the design of experiments at a graphical interface and generates computer-readable metadata files, which capture information about genotypes, growth conditions, environmental perturbations and sampling strategy.
    Plant Cell Environ. 2009 Sep;32(9):1185-200 PMID: 19236607
  19. Description and applications of a rapid and sensitive non-radioactive microplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase.
    Plant Cell Environ. 2007 Sep;30(9):1163-75 PMID: 17661753
  20. A network of multiple regulatory layers shapes gene expression in fission yeast.
    Mol Cell. 2007 Apr 13;26(1):145-55 PMID: 17434133
  21. Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts.
    Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6466-71 PMID: 17404229
  22. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  23. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata.
    Mol Biol Evol. 2004 Sep;21(9):1719-26 PMID: 15201397
  24. GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after 13CO2 labelling.
    Phytochemistry. 2007 Aug-Sep;68(16-18):2258-72 PMID: 17475294
  25. Determinants of RNA quality from FFPE samples.
    PLoS One. 2007 Dec 05;2(12):e1261 PMID: 18060057
  26. Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome.
    RNA. 2007 Jul;13(7):982-97 PMID: 17586758
  27. Regulation of protein synthesis at the elongation stage. New insights into the control of gene expression in eukaryotes.
    FEBS Lett. 1991 Jul 22;285(2):170-5 PMID: 1855586
  28. Global analyses of mRNA translational control during early Drosophila embryogenesis.
    Genome Biol. 2007;8(4):R63 PMID: 17448252
  29. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana.
    Plant J. 2004 Jun;38(5):823-39 PMID: 15144383
  30. 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. 2009 Jul;32(7):859-74 PMID: 19236606
  31. Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis.
    Plant Cell Environ. 2009 Mar;32(3):300-18 PMID: 19054347
  32. Regulation of hemoglobin synthesis. Equal rates of translation and termination of - and -globin chains.
    J Biol Chem. 1972 Jun 10;247(11):3622-9 PMID: 4624122
  33. Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers.
    J Exp Bot. 2001 Oct;52(363):1981-9 PMID: 11559733
  34. A mechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3881-5 PMID: 8632983
  35. Measurement of Protein Degradation in Leaves of Zea mays Using [H]Acetic Anhydride and Tritiated Water.
    Plant Physiol. 1981 Jun;67(6):1214-9 PMID: 16661839
  36. Codon usage and gene function are related in sequences of Arabidopsis thaliana.
    Gene. 1998 Mar 16;209(1-2):GC1-GC38 PMID: 9583944
  37. The 'effective number of codons' used in a gene.
    Gene. 1990 Mar 1;87(1):23-9 PMID: 2110097
  38. Ribosome pausing and stacking during translation of a eukaryotic mRNA.
    EMBO J. 1988 Nov;7(11):3559-69 PMID: 2850168
  39. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3889-94 PMID: 12660367
  40. Increase in respiratory cost at high growth temperature is attributed to high protein turnover cost in Petunia x hybrida petals.
    Plant Cell Environ. 2007 Oct;30(10):1269-83 PMID: 17727417
  41. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.
    Plant Cell. 2005 Dec;17(12):3257-81 PMID: 16299223
  42. Escherichia coli UMP-kinase, a member of the aspartokinase family, is a hexamer regulated by guanine nucleotides and UTP.
    Biochemistry. 1995 Apr 18;34(15):5066-74 PMID: 7711027
  43. Cost of protein synthesis and energy allocation during development of antarctic sea urchin embryos and larvae.
    Biol Bull. 2007 Apr;212(2):115-29 PMID: 17438204
  44. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro.
    J Exp Bot. 2002 Jan;53(366):103-10 PMID: 11741046
  45. E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI).
    BMC Bioinformatics. 2008 Jan 29;9:65 PMID: 18230160
  46. Chloroplast translation regulation.
    Photosynth Res. 2007 Nov-Dec;94(2-3):359-74 PMID: 17661159
  47. mRNA sequence features that contribute to translational regulation in Arabidopsis.
    Nucleic Acids Res. 2005 Feb 16;33(3):955-65 PMID: 15716313
  48. 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 ADP-glucose pyrophosphorylase in the following light period.
    Plant J. 2004 Sep;39(6):847-62 PMID: 15341628
  49. Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions.
    Plant Physiol. 2006 Dec;142(4):1574-88 PMID: 17085515
  50. NAD malic enzyme and the control of carbohydrate metabolism in potato tubers.
    Plant Physiol. 2001 Jul;126(3):1139-49 PMID: 11457964
  51. Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes.
    Genome Biol. 2006;7(8):R76 PMID: 16916443
  52. 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. 2004 Sep;136(1):2687-99 PMID: 15347792
  53. An evolutionary perspective on synonymous codon usage in unicellular organisms.
    J Mol Evol. 1986;24(1-2):28-38 PMID: 3104616
  54. The ubiquitin-26S proteasome system at the nexus of plant biology.
    Nat Rev Mol Cell Biol. 2009 Jun;10(6):385-97 PMID: 19424292
  55. CSB.DB: a comprehensive systems-biology database.
    Bioinformatics. 2004 Dec 12;20(18):3647-51 PMID: 15247097
  56. The economics of ribosome biosynthesis in yeast.
    Trends Biochem Sci. 1999 Nov;24(11):437-40 PMID: 10542411
  57. 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. 2005 Sep;4(9):1265-72 PMID: 15958392
  58. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm.
    Plant Physiol. 2007 Oct;145(2):513-26 PMID: 17720759
  59. Balanced production of ribosomal proteins.
    Gene. 2007 Oct 15;401(1-2):1-3 PMID: 17689889
  60. 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. 1997;203(3):304-19 PMID: 9431679
  61. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis.
    Plant Physiol. 2005 Sep;139(1):5-17 PMID: 16166256
  62. Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function.
    Plant J. 2007 Jun;50(6):1093-106 PMID: 17461782
  63. Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone.
    Mol Cell Proteomics. 2004 May;3(5):478-89 PMID: 14766929
  64. Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes.
    Plant Physiol. 2008 Apr;146(4):1834-61 PMID: 18305208
  65. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.
    Neurosci Lett. 2003 Mar 13;339(1):62-6 PMID: 12618301
  66. Translational profiling: the genome-wide measure of the nascent proteome.
    Brief Funct Genomic Proteomic. 2004 Aug;3(2):103-11 PMID: 15355593
  67. Molecular and biochemical characterization of cytosolic phosphoglucomutase in maize. Expression during development and in response to oxygen deprivation.
    Plant Physiol. 1998 Jul;117(3):997-1006 PMID: 9662542
  68. Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana.
    Genome Biol. 2008;9(8):R129 PMID: 18710526
Article Info
Journal
Molecular systems biology
Abbr.
Mol Syst Biol
ISSN
1744-4292
Published
2009-00-00
Epub
2009-00-13
Pages
314
Language
English
Region
England
NLM ID
101235389
PMCID
PMC2779082
Subset
IM
Analysis Services
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