High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions

Plant Journal

Volumn 67, Issue 5, 2011, Pages 869-884

  Caldana, Camila ^a   Degenkolbe, Thomas ^a   Cuadros Inostroza, Alvaro ^a   Klie, Sebastian ^a   Sulpice, Ronan ^a   Leisse, Andrea ^a   Steinhauser, Dirk ^a   Fernie, Alisdair R ^a   Willmitzer, Lothar ^a   Hannah, Matthew A ^a,b  

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

^b Bayer sa nv Belgium   (Belgium)

Author keywords

abiotic stress; kinetics; metabolome; protein degradation; transcriptome

Indexed keywords

ABIOTIC STRESS; ARABIDOPSIS; ARABIDOPSIS THALIANA; CELLULAR ENERGY; ELECTRON TRANSFER; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL PERTURBATIONS; GENE ONTOLOGY; HIERARCHICAL CLUSTER ANALYSIS; HIGH-DENSITY; KINETIC ANALYSIS; LIGHT INTENSITY; LOGARITHMIC TIME; METABOLIC NETWORK; METABOLOMES; METABOLOMICS; PARALLEL ANALYSIS; PROTEIN DEGRADATION; TIME POINTS; TIME-RESOLVED; TRANSCRIPTIONAL CHANGES; TRANSCRIPTIONAL RESPONSE; TRANSCRIPTOMES; TRICARBOXYLIC ACID CYCLE;

AMINO ACIDS; CLUSTER ANALYSIS; DEGRADATION; GENES; HIERARCHICAL SYSTEMS; METABOLISM; METABOLITES; ONTOLOGY; TIME SERIES;

KINETICS;

FLAVOPROTEIN; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; CLUSTER ANALYSIS; DARKNESS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; KINETICS; LIGHT; METABOLISM; METABOLOME; METABOLOMICS; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN DEGRADATION; RADIATION EXPOSURE; TEMPERATURE; TIME;

ARABIDOPSIS; CLUSTER ANALYSIS; DARKNESS; FLAVOPROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; KINETICS; LIGHT; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOSYNTHESIS; PROTEOLYSIS; TEMPERATURE; TIME FACTORS; TRANSCRIPTOME;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80052272064     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04640.x     Document Type: Article

References (69)

1. Araujo, W.L., Ishizaki, K., Nunes-Nesi, A., et al. (2010) Identification of the 2-Hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell, 22, 1549-1563.
2. Baena-Gonzalez, E., and, Sheen, J., (2008) Convergent energy and stress signaling. Trends Plant Sci. 13, 474-482.
3. Bieniawska, Z., Espinoza, C., Schlereth, A., Sulpice, R., Hincha, D.K., and, Hannah, M.A., (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 147, 263-279. (Pubitemid 352844361)
4. Blasing, O.E., Gibon, Y., Gunther, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.R., and, 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.
5. Bown, A.W., and, Shelp, B.J., (1997) The metabolism and functions of gamma-aminobutyric acid. Plant Physiol. 115, 1-5.
6. Bradley, P.H., Brauer, M.J., Rabinowitz, J.D., and, Troyanskaya, O.G., (2009) Coordinated concentration changes of transcripts and metabolites in Saccharomyces cerevisiae. PLoS Comput. Biol. 5, 15.
7. Caldana, C., Scheible, W.R., Mueller-Roeber, B., and, Ruzicic, S., (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods, 3, 9.
8. Cook, D., Fowler, S., Fiehn, O., and, Thomashow, M.F., (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl Acad. Sci. USA, 101, 15243-15248. (Pubitemid 39391749)
9. Cuadros-Inostroza, A., Caldana, C., Redestig, H., Kusano, M., Lisec, J., Pena-Cortes, H., Willmitzer, L., and, Hannah, M.A., (2009) TargetSearch-a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics, 10, 12.
10. 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. (Pubitemid 43951587)
11. Diaz-Troya, S., Perez-Perez, M.E., Florencio, F.J., and, Crespo, J.L., (2008) The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy, 4, 851-865.
12. Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J., and, Webb, A.A.R., (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630-633. (Pubitemid 41033650)
13. Espinosa, C., Degenkolbe, T., Caldana, C., Zuther, E., Leisse, A., Willmitzer, L., Hincha, D, and, Hannah, M., (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLos ONE, 5 (11), e14101.
14. Fowler, S., and, Thomashow, M.F., (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell, 14, 1675-1690. (Pubitemid 35002928)
15. Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Nishida, I., and, Watanabe, A., (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol. Plant. 111, 345-352.
16. Gautier, L., Cope, L., Bolstad, B.M., and, Irizarry, R.A., (2004) Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics, 20, 307-315. (Pubitemid 38262761)
17. Gentleman, R., Carey, V., Bates, D., et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
18. Gibon, Y., Usadel, B., Blaesing, O.E., Kamlage, B., Hoehne, M., Trethewey, R., and, Stitt, M., (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol. 7, 23.
19. Guy, C., Kaplan, F., Kopka, J., Selbig, J., and, Hincha, D.K., (2008) Metabolomics of temperature stress. Physiol. Plant. 132, 220-235.
20. Hannah, M.A., Heyer, A.G., and, Hincha, D.K., (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet. 1, e26.
21. Hannah, M.A., Wiese, D., Freund, S., Fiehn, O., Heyer, A.G., and, Hincha, D.K., (2006) Natural genetic variation of freezing tolerance in arabidopsis. Plant Physiol. 142, 98-112. (Pubitemid 44412233)
22. Hannah, M.A., Redestig, H., Leisse, A., and, Willmitzer, L., (2008) Global mRNA changes in microarray experiments. Nat. Biotechnol. 26, 741-742. (Pubitemid 351961441)
23. Hirai, M.Y., Yano, M., Goodenowe, D.B., Kanaya, S., Kimura, T., Awazuhara, M., Arita, M., Fujiwara, T., and, Saito, K., (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 101, 10205-10210. (Pubitemid 38891220)
24. Ishii, N., Nakahigashi, K., Baba, T., et al. (2007) Multiple high-throughput analyses monitor the response of E-coli to perturbations. Science, 316, 593-597. (Pubitemid 46683144)
25. Ishizaki, K., Larson, T.R., Schauer, N., Fernie, A.R., Graham, I.A., and, Leaver, C.J., (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell, 17, 2587-2600.
26. Ishizaki, K., Schauer, N., Larson, T.R., Graham, I.A., Fernie, A.R., and, Leaver, C.J., (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J. 47, 751-760. (Pubitemid 44215440)
27. Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y., and, Guy, C.L., (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136, 4159-4168.
28. Kaplan, F., Kopka, J., Sung, D.Y., Zhao, W., Popp, M., Porat, R., and, Guy, C.L., (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J. 50, 967-981. (Pubitemid 46904105)
29. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., Dángelo, C., Bornberg-Bauer, E., Kudla, J., and, Harter, K., (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363. (Pubitemid 46624141)
30. Kinnersley, A.M., and, Turano, F.J., (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit. Rev. Plant Sci. 19, 479-509.
31. Kojima, H., Suzuki, T., Kato, T., et al. (2007) Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development. Plant J. 49, 1053-1063. (Pubitemid 46340697)
32. Krouk, G., Tranchina, D., Lejay, L., Cruikshank, A.A., Shasha, D., Coruzzi, G.M., and, Gutiárrez, R.A., (2009) A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Comput. Biol. 5, e1000326.
33. Kusano, M., Fukushima, A., Arita, M., Jonsson, P., Moritz, T., Kobayashi, M., Hayashi, N., Tohge, T., and, Saito, K., (2007) Unbiased characterization of genotype-dependent metabolic regulations by metabolomic approach in Arabidopsis thaliana. BMC Syst. Biol. 1, 53.
34. Lamesch, P., Dreher, K., Swarbreck, D., Sasidharan, R., Reiser, L., and, Huala, E., (2010) Using the Arabidopsis information resource (TAIR) to find information about Arabidopsis genes. Curr. Protoc. Bioinformatics, Chapter 1, Unit1.11.
35. Langfelder, P., and, Horvath, S.,. (2008) WGCNA: an R package for weighted gene co-expression network analysis. BMC Bioinformatics, 9, 559, doi:10.1186/1471-2105-9-559.
36. Less, H., and, Galili, G., (2009) Coordinations between gene modules control the operation of plant amino acid metabolic networks. BMC Syst. Biol. 3, 18.
37. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and, Fernie, A.R., (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396.
38. Maruyama, K., Takeda, M., Kidokoro, S., et al. (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150, 1972-1980.
39. Matsuda, F., Hirai, M.Y., Sasaki, E., Akiyama, K., Yonekura-Sakakibara, K., Provart, N.J., Sakurai, T., Shimada, Y., and, Saito, K., (2010) AtMetExpress development: a phytochemical atlas of Arabidopsis development. Plant Physiol. 152, 566-578.
40. Michael, T.P., Breton, G., Hazen, S.P., Priest, H., Mockler, T.C., Kay, S.A., and, Chory, J., (2008) A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol. 6, 1887-1898.
41. Mittler, R., (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19. (Pubitemid 43053973)
42. Mueller, L.A., Zhang, P.F., and, Rhee, S.Y., (2003) AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol. 132, 453-460. (Pubitemid 36715048)
43. Ralser, M., Wamelink, M.M.C., Latkolik, S., Jansen, E.E.W., Lehrach, H., and, Jakobs, C., (2009) Metabolic reconfiguration precedes transcriptional regulation in the antioxidant response. Nat Biotechnol. 27, 604-605.
44. Redestig, H., Weicht, D., Selbig, J., and, Hannah, M.A., (2007) Transcription factor target prediction using multiple short expression time series from Arabidopsis thaliana. BMC Bioinformatics, 8, 16.
45. Schmelzle, T., and, Hall, M.N., (2000) TOR, a central controller of cell growth. Cell, 103, 253-262.
46. Seki, M., Narusaka, M., Ishida, J., et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292. (Pubitemid 34922963)
47. Smeekens, S., Ma, J.K., Hanson, J., and, Rolland, F., (2010) Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant Biol. 13, 274-279.
48. Southam, A.D., Easton, J.M., Stentiford, G.D., Ludwig, C., Arvanitis, T.N., and, Viant, M.R., (2008) Metabolic changes in flatfish hepatic tumours revealed by NMR-based metabolomics and metabolic correlation networks. J. Proteome Res. 7, 5277-5285.
49. Stacklies, W., Redestig, H., Scholz, M., Walther, D., and, Selbig, J., (2007) pcaMethods a bioconductor package providing PCA methods for incomplete data. Bioinformatics, 23, 1164-1167. (Pubitemid 47050571)
50. Stitt, M., Sulpice, R., Gibon, Y., Whitwell, A., Skilbeck, R., Parker, S., and, Ellison, R., (2007) Cryogenic grinder system. Germany: Patent No. 08146.0025U1.
51. Strayer, C., Oyama, T., Schultz, T.F., Raman, R., Somers, D.E., Mas, P., Panda, S., Kreps, J.A., and, Kay, S.A., (2000) Cloning of the Arabidopsis clock cone TOC1, an autoregulatory response regulator homolog. Science, 289, 768-771. (Pubitemid 30650195)
52. Studart-Guimaraes, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B., and, Fernie, A.R., (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol. 145, 626-639. (Pubitemid 350127596)
53. Sung, D.Y., Vierling, E., and, Guy, C.L., (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126, 789-800. (Pubitemid 32568814)
54. Suzuki, R., and, Shimodaira, H., (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540-1542. (Pubitemid 43985330)
55. Szymanski, J., Jozefczuk, S., Nikoloski, Z., Selbig, J., Nikiforova, V., Catchpole, G., and, Willmitzer, L., (2009) Stability of metabolic correlations under changing environmental conditions in Escherichia coli- a systems approach. PLoS one, 4 (10), e7441. doi:10.1371/journal.pone.0007441
56. Taylor, N.L., Heazlewood, J.L., Day, D.A., and, Millar, A.H., (2004) Lipoic acid-dependent oxidative catabolism of alpha-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol. 134, 838-848. (Pubitemid 38261555)
57. Thomashow, M.F., (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599. (Pubitemid 129491974)
58. Thompson, A.R., and, Vierstra, R.D., (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr. Opin. Plant Biol. 8, 165-173. (Pubitemid 40323546)
59. Thum, K.E., Shin, M.J., Gutierrez, R.A., Mukherjee, I., Katari, M.S., Nero, D., Shasha, D., and, Coruzzi, G.M., (2008a) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst. Biol. 2, Article No.: 31.
60. Thum, K.E., Shin, M.J., Gutierrez, R.A., Mukherjee, I., Katari, M.S., Nero, D., Shasha, D., and, Coruzzi, G.M., (2008b) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst. Biol. 2, 19.
61. Tong, C.G., Reichler, S., Blumenthal, S., Balk, J., Hsieh, H.L., and, Roux, S.J., (1997) Light regulation of the abundance of mRNA encoding a nucleolin-like protein localized in the nucleoli of pea nuclei. Plant Physiol. 114, 643-652. (Pubitemid 28378556)
62. Usadel, B., Nagel, A., Steinhauser, D., et al. (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics, 7, 535.
63. Usadel, B., Bläsing, O., Gibon, Y., Poree, F., Höhne, M., Günter, M., Trethewey, R., Kamlage, B., Poorter, H., and, Stitt, M., (2008) Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 31, 518-547. (Pubitemid 351388642)
64. Weckwerth, W., Loureiro, M.E., Wenzel, K., and, Fiehn, O., (2004a) Differential metabolic networks unravel the effects of silent plant phenotypes. Proc. Natl Acad. Sci. USA, 101, 7809-7814. (Pubitemid 38658110)
65. Weckwerth, W., Wenzel, K., and, Fiehn, O., (2004b) Process for the integrated extraction identification, and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics, 4, 78-83. (Pubitemid 38140876)
66. Weigelt, K., Kuster, H., Radchuk, R., Muller, M., Weichert, H., Fait, A., Fernie, A.R., Saalbach, I., and, Weber, H., (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J. 55, 909-926.
67. Wu, Z.J., Irizarry, R.A., Gentleman, R., Martinez-Murillo, F., and, Spencer, F., (2004) A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99, 909-917. (Pubitemid 39665934)
68. Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T., and, Ohsumi, Y., (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell, 16, 2967-2983. (Pubitemid 41075746)
69. Zhang, B., and, Horvath, S., (2005) A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol. 4 (1), Article 17.