Metabolic configuration and adaptation under a range of abiotic stresses, including drought, heat, salinity, cold, and nutrient deprivation, are subjected to an intricate span of molecular pathways that work in parallel in order to enhance plant fitness and increase stress tolerance. In recent years, unprecedented advances have been made in identifying and linking different abiotic stresses, and the current challenge in plant molecular biology is deciphering how the signaling responses are integrated and transduced throughout metabolism. Metabolomics have often played a fundamental role in elucidating the distinct and overlapping biochemical changes that occur in plants. However, a far greater understanding and appreciation of the complexity in plant metabolism under specific stress conditions have become apparent when combining metabolomics with other—omic platforms. This review focuses on recent advances made in understanding the global changes occurring in plant metabolism under abiotic stress conditions using metabolite profiling as an integrated discovery platform.
Skirycz, A.; Vandenbroucke, K.; Clauw, P.; Maleux, K.; De Meyer, B.; Dhondt, S.; Pucci, A.; Gonzalez, N.; Hoeberichts, F.; Tognetti, V.B.; et al. Survival and growth of arabidopsis plants given limited water are not equal. Nat. Biotechnol. 2011, 29, 212–214, doi:10.1038/nbt.1800.
[3]
Claeys, H.; Skirycz, A.; Maleux, K.; Inzé, D. Della signaling mediates stress-induced cell differentiation in arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol. 2012, 159, 739–747, doi:10.1104/pp.112.195032.
[4]
Skirycz, A.; Claeys, H.; De Bodt, S.; Oikawa, A.; Shinoda, S.; Andriankaja, M.; Maleux, K.; Eloy, N.B.; Coppens, F.; Yoo, S.-D.; et al. Pause-and-stop: The effects of osmotic stress on cell proliferation during early leaf development in arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell. 2011, 23, 1876–1888, doi:10.1105/tpc.111.084160.
[5]
Levey, S.; Wingler, A. Natural variation in the regulation of leaf senescence and relation to other traits in arabidopsis. Plant Cell. Environ. 2005, 28, 223–231, doi:10.1111/j.1365-3040.2004.01266.x.
[6]
Qin, F.; Kodaira, K.-S.; Maruyama, K.; Mizoi, J.; Tran, L.-S.P.; Fujita, Y.; Morimoto, K.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Spindly, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol. 2011, 157, 1900–1913, doi:10.1104/pp.111.187302.
[7]
Munns, R. Comparative physiology of salt and water stress. Plant Cell. Environ. 2002, 25, 239–250, doi:10.1046/j.0016-8025.2001.00808.x.
[8]
Wingler, A.; Roitsch, T. Metabolic regulation of leaf senescence: Interactions of sugar signalling with biotic and abiotic stress responses. Plant Biology 2008, 10, 50–62, doi:10.1111/j.1438-8677.2008.00086.x.
[9]
Kesari, R.; Lasky, J.R.; Villamor, J.G.; Des Marais, D.L.; Chen, Y.-J.C.; Liu, T.-W.; Lin, W.; Juenger, T.E.; Verslues, P.E. Intron-mediated alternative splicing of arabidopsis p5cs1 and its association with natural variation in proline and climate adaptation. Proc. Natl. Acad. Sci. USA 2012, 109, 9197–9202, doi:10.1073/pnas.1203433109.
[10]
Yoshiba, Y.; Kiyosue, T.; Katagiri, T.; Ueda, H.; Mizoguchi, T.; Yamaguchi-Shinozaki, K.; Wada, K.; Harada, Y.; Shinozaki, K. Correlation between the induction of a gene for δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in arabidopsis thaliana under osmotic stress. Plant J. 1995, 7, 751–760.
[11]
Waditee, R.; Bhuiyan, M.N.H.; Rai, V.; Aoki, K.; Tanaka, Y.; Hibino, T.; Suzuki, S.; Takano, J.; Jagendorf, A.T.; Takabe, T.; et al. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in synechococcus and arabidopsis. Proc. Natl. Acad. Sci. USA 2005, 102, 1318–1323, doi:10.1073/pnas.0409017102.
[12]
Ioannidis, N.E.; Cruz, J.A.; Kotzabasis, K.; Kramer, D.M. Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS one 2012, 7, e29864.
Cuevas, J.C.; López-Cobollo, R.; Alcázar, R.; Zarza, X.; Koncz, C.; Altabella, T.; Salinas, J.; Tiburcio, A.F.; Ferrando, A. Putrescine is involved in arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol. 2008, 148, 1094–1105, doi:10.1104/pp.108.122945.
[15]
Renault, H.; El Amrani, A.; Berger, A.; Mouille, G.; Soubigou-Taconnat, L.; Bouchereau, A.; Deleu, C. Γ-aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in arabidopsis roots. Plant Cell. Environ. 2013, 36, 1009–1018, doi:10.1111/pce.12033.
[16]
Van Dongen, J.T.; Fr?hlich, A.; Ramírez-Aguilar, S.J.; Schauer, N.; Fernie, A.R.; Erban, A.; Kopka, J.; Clark, J.; Langer, A.; Geigenberger, P. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of arabidopsis plants. Ann. Bot. 2009, 103, 269–280.
[17]
Osuna, D.; Usadel, B.; Morcuende, R.; Gibon, Y.; Bl?sing, O.E.; H?hne, M.; Günter, M.; Kamlage, B.; Trethewey, R.; Scheible, W.-R.; et al. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived arabidopsis seedlings. Plant J. 2007, 49, 463–491, doi:10.1111/j.1365-313X.2006.02979.x.
[18]
Raschke, M.; Boycheva, S.; Crèvecoeur, M.; Nunes-Nesi, A.; Witt, S.; Fernie, A.R.; Amrhein, N.; Fitzpatrick, T.B. Enhanced levels of vitamin b6 increase aerial organ size and positively affect stress tolerance in arabidopsis. Plant J. 2011, 66, 414–432, doi:10.1111/j.1365-313X.2011.04499.x.
[19]
Tunc-Ozdemir, M.; Miller, G.; Song, L.; Kim, J.; Sodek, A.; Koussevitzky, S.; Misra, A.N.; Mittler, R.; Shintani, D. Thiamin confers enhanced tolerance to oxidative stress in arabidopsis. Plant Physiol. 2009, 151, 421–432, doi:10.1104/pp.109.140046.
[20]
Miller, G.; Suzuki, N.; Rizhsky, L.; Hegie, A.; Koussevitzky, S.; Mittler, R. Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol. 2007, 144, 1777–1785, doi:10.1104/pp.107.101436.
[21]
Szarka, A.; Tomasskovics, B.; Bánhegyi, G. The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int. J. Mol. Sci. 2012, 13, 4458–4483, doi:10.3390/ijms13044458.
[22]
Suzuki, N.; Koussevitzky, S.; Mittler, R.O.N.; Miller, G.A.D. Ros and redox signalling in the response of plants to abiotic stress. Plant Cell. Environ. 2012, 35, 259–270, doi:10.1111/j.1365-3040.2011.02336.x.
[23]
Urano, K.; Maruyama, K.; Ogata, Y.; Morishita, Y.; Takeda, M.; Sakurai, N.; Suzuki, H.; Saito, K.; Shibata, D.; Kobayashi, M.; et al. Characterization of the aba-regulated global responses to dehydration in arabidopsis by metabolomics. Plant J. 2009, 57, 1065–1078, doi:10.1111/j.1365-313X.2008.03748.x.
[24]
Saito, K.; Matsuda, F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu Rev. Plant Biol 2010, 61, 463–489, doi:10.1146/annurev.arplant.043008.092035.
[25]
Fraire-Velázquez, S.; Balderas-Hernández, V.E. Abiotic stress in plants and metabolic responses. In Abiotic Stress—Plant Responses and Applications in Agriculture; Vahdati, K, Leslie, C., Eds.; Intechopen, 2013. doi:10.5772/54859.
[26]
Obata, T.; Fernie, A. The use of metabolomics to dissect plant responses to abiotic stresses. Cell. Mol. Life Sci. 2012, 69, 3225–3243, doi:10.1007/s00018-012-1091-5.
[27]
Kueger, S.; Steinhauser, D.; Willmitzer, L.; Giavalisco, P. High-resolution plant metabolomics: From mass spectral features to metabolites and from whole-cell analysis to subcellular metabolite distributions. Plant J. 2012, 70, 39–50, doi:10.1111/j.1365-313X.2012.04902.x.
[28]
Hur, M.; Campbell, A.A.; Almeida-de-Macedo, M.; Li, L.; Ransom, N.; Jose, A.; Crispin, M.; Nikolau, B.J.; Wurtele, E.S. A global approach to analysis and interpretation of metabolic data for plant natural product discovery. Nat. Prod. Rep. 2013, 30, 565–583, doi:10.1039/c3np20111b.
[29]
Narsai, R.; Howell, K.A.; Carroll, A.; Ivanova, A.; Millar, A.H.; Whelan, J. Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol. 2009, 151, 306–322, doi:10.1104/pp.109.142026.
[30]
Ralston-Hooper, K.; Jannasch, A.; Adamec, J.; Sepúlveda, M. The use of two-dimensional gas chromatography–time-of-flight mass spectrometry (gc× gc–tof-ms) for metabolomic analysis of polar metabolites. In Metabolic Profiling; 2011; Volume 708, pp. 205–211.
[31]
Little, J.L. Artifacts in trimethylsilyl derivatization reactions and ways to avoid them. J. Chromatogr A 1999, 844, 1–22, doi:10.1016/S0021-9673(99)00267-8.
[32]
Halket, J.M.; Waterman, D.; Przyborowska, A.M.; Patel, R.K.P.; Fraser, P.D.; Bramley, P.M. Chemical derivatization and mass spectral libraries in metabolic profiling by gc/ms and lc/ms/ms. J. Exp. Bot. 2005, 56, 219–243.
[33]
Golm metabolome Database (GMD). Available online: http://gmd.mpimp-golm.mpg.de/ (accessed on 27 June 2013).
[34]
Giavalisco, P.; Li, Y.; Matthes, A.; Eckhardt, A.; Hubberten, H.-M.; Hesse, H.; Segu, S.; Hummel, J.; K?hl, K.; Willmitzer, L. Elemental formula annotation of polar and lipophilic metabolites using 13c, 15n and 34s isotope labelling, in combination with high-resolution mass spectrometry. Plant J. 2011, 68, 364–376, doi:10.1111/j.1365-313X.2011.04682.x.
[35]
Leng, J.; Wang, H.; Zhang, L.; Zhang, J.; Guo, Y. A highly sensitive isotope-coded derivatization method and its application for the mass spectrometric analysis of analytes containing the carboxyl group. Anal. Chim. Acta. 2013, 758, 114–121, doi:10.1016/j.aca.2012.11.008.
[36]
Gaquerel, E.; Kuhl, C.; Neumann, S. Computational annotation of plant metabolomics profiles via a novel network-assisted approach. Metabolomics 2013, 1–15.
[37]
Metabolomic Tool Kit —GARnet. Available online: http://www.garnetcommunity.org.uk/resources/metabolomic-tool-kit/ (accessed on 27 June 2013).
[38]
Pathway Activity Profiling (PAPi). Available online: http://www.4shared.com/file/s0uIYWIg/PAPi_10.html/ (accessed on 29 June 2013).
[39]
Metabolites Biological Role. Available online: http://pdg.cnb.uam.es/mbrole/ (accessed on 26 July 2013).
[40]
Fukushima, A.; Kusano, M.; Redestig, H.; Arita, M.; Saito, K. Metabolomic correlation-network modules in arabidopsis based on a graph-clustering approach. BMC Syst Biol 2011, 5, 1, doi:10.1186/1752-0509-5-1.
[41]
Saito, K.; Hirai, M.Y.; Yonekura-Sakakibara, K. Decoding genes with coexpression networks and metabolomics—“Majority report by precogs”. Trends Plant Sci. 2008, 13, 36–43, doi:10.1016/j.tplants.2007.10.006.
[42]
Scholz, M.; Gatzek, S.; Sterling, A.; Fiehn, O.; Selbig, J. Metabolite fingerprinting: Detecting biological features by independent component analysis. Bioinformatics 2004, 20, 2447–2454, doi:10.1093/bioinformatics/bth270.
[43]
Redestig, H.; Costa, I.G. Detection and interpretation of metabolite–transcript coresponses using combined profiling data. Bioinformatics 2011, 27, i357–i365, doi:10.1093/bioinformatics/btr231.
[44]
Kamburov, A.; Cavill, R.; Ebbels, T.M.D.; Herwig, R.; Keun, H.C. Integrated pathway-level analysis of transcriptomics and metabolomics data with impala. Bioinformatics 2011, 27, 2917–2918, doi:10.1093/bioinformatics/btr499.
[45]
IMPaLA: Integrated Molecular Pathway Level Analysis. Available online: http://impala.molgen.mpg.de/ (accessed on 26 June 2013).
[46]
Painting omics data in biological pathways. Available online: http://www.paintomics.org/cgi-bin/main2.cgi/ (accessed on 29 June 2013).
[47]
Sulpice, R.; Trenkamp, S.; Steinfath, M.; Usadel, B.; Gibon, Y.; Witucka-Wall, H.; Pyl, E.-T.; Tschoep, H.; Steinhauser, M.C.; Guenther, M.; et al. Network analysis of enzyme activities and metabolite levels and their relationship to biomass in a large panel of arabidopsis accessions. Plant Cell. 2010, 22, 2872–2893, doi:10.1105/tpc.110.076653.
[48]
Cross, J.M.; von Korff, M.; Altmann, T.; Bartzetko, L.; Sulpice, R.; Gibon, Y.; Palacios, N.; Stitt, M. Variation of enzyme activities and metabolite levels in 24 arabidopsis accessions growing in carbon-limited conditions. Plant Physiol. 2006, 142, 1574–1588, doi:10.1104/pp.106.086629.
[49]
Gibon, Y.; Usadel, B.; Blaesing, O.; Kamlage, B.; Hoehne, M.; Trethewey, R.; Stitt, M. Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in arabidopsis rosettes. Genome Biol. 2006, 7, R76, doi:10.1186/gb-2006-7-8-r76.
[50]
Hirai, M.Y.; Yano, M.; Goodenowe, D.B.; Kanaya, S.; Kimura, T.; Awazuhara, M.; Arita, M.; Fujiwara, T.; Saito, K. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2004, 101, 10205–10210, doi:10.1073/pnas.0403218101.
[51]
Fernie, A.R.; Stitt, M. On the discordance of metabolomics with proteomics and transcriptomics: Coping with increasing complexity in logic, chemistry and network interactions. Plant Physiol. 2012, 158, 1139–1145, doi:10.1104/pp.112.193235.
[52]
Hannah, M.A.; Caldana, C.; Steinhauser, D.; Balbo, I.; Fernie, A.R.; Willmitzer, L. Combined transcript and metabolite profiling of arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol. 2010, 152, 2120–2129, doi:10.1104/pp.109.147306.
[53]
Gouws, L.; Botes, E.; Wiese, A.J.; Trenkamp, S.; Torres-Jerez, I.; Tang, Y.; Hills, P.N.; Usadel, B.; Lloyd, J.R.; Fernie, A.; et al. The plant growth promoting substance, lumichrome, mimics starch and ethylene-associated symbiotic responses in lotus and tomato roots. Front. Plant Sci 2012, doi:10.3389/fpls.2012.00120.
[54]
Espinoza, C.; Degenkolbe, T.; Caldana, C.; Zuther, E.; Leisse, A.; Willmitzer, L.; Hincha, D.K.; Hannah, M.A. Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in arabidopsis. PLoS One 2010, 5, e14101, doi:10.1371/journal.pone.0014101.
[55]
Ndamukong, I.; Jones, D.R.; Lapko, H.; Divecha, N.; Avramova, Z. Phosphatidylinositol 5-phosphate links dehydration stress to the activity of arabidopsis trithorax-like factor atx1. PLoS One 2010, 5, e13396.
[56]
Saleh, A.; Alvarez-Venegas, R.; Yilmaz, M.; Le, O.; Hou, G.; Sadder, M.; Al-Abdallat, A.; Xia, Y.; Lu, G.; Ladunga, I.; et al. The highly similar arabidopsis homologs of trithorax atx1 and atx2 encode proteins with divergent biochemical functions. Plant Cell. 2008, 20, 568–579, doi:10.1105/tpc.107.056614.
[57]
Pien, S.; Fleury, D.; Mylne, J.S.; Crevillen, P.; Inzé, D.; Avramova, Z.; Dean, C.; Grossniklaus, U. Arabidopsis trithorax1 dynamically regulates flowering locus c activation via histone 3 lysine 4 trimethylation. Plant Cell. 2008, 20, 580–588, doi:10.1105/tpc.108.058172.
[58]
Pical, C.; Westergren, T.; Dove, S.K.; Larsson, C.; Sommarin, M. Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in arabidopsis thaliana cells. J. Biol. Chem. 1999, 274, 38232–38240.
[59]
Ndamukong, I.; Lapko, H.; Cerny, R.L.; Avramova, Z. A cytoplasm-specific activity encoded by the trithorax-like atx1 gene. Nucleic Acids Res. 2011, 39, 4709–4718, doi:10.1093/nar/gkq1300.
[60]
Li, J.; Brader, G.; Palva, E.T. The wrky70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell. 2004, 16, 319–331, doi:10.1105/tpc.016980.
[61]
Besseau, S.; Li, J.; Palva, E.T. Wrky54 and wrky70 co-operate as negative regulators of leaf senescence in arabidopsis thaliana. J. Exp. Bot. 2012, 63, 2667–2679, doi:10.1093/jxb/err450.
[62]
Yao, Y.; Kovalchuk, I. Abiotic stress leads to somatic and heritable changes in homologous recombination frequency, point mutation frequency and microsatellite stability in arabidopsis plants. Mutat. Res.—Fund. Mol. M. 2011, 707, 61–66, doi:10.1016/j.mrfmmm.2010.12.013.
[63]
Weinberg, Z.; Wang, J.; Bogue, J.; Yang, J.; Corbino, K.; Moy, R.; Breaker, R. Comparative genomics reveals 104 candidate structured rnas from bacteria, archaea, and their metagenomes. Genome Biol. 2010, 11, R31, doi:10.1186/gb-2010-11-3-r31.
[64]
Bocobza, S.; Adato, A.; Mandel, T.; Shapira, M.; Nudler, E.; Aharoni, A. Riboswitch-dependent gene regulation and its evolution in the plant kingdom. Genes Dev. 2007, 21, 2874–2879, doi:10.1101/gad.443907.
[65]
Wachter, A.; Tunc-Ozdemir, M.; Grove, B.C.; Green, P.J.; Shintani, D.K.; Breaker, R.R. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mrnas. Plant Cell. 2007, 19, 3437–3450, doi:10.1105/tpc.107.053645.
[66]
Bocobza, S.E.; Malitsky, S.; Araújo, W.L.; Nunes-Nesi, A.; Meir, S.; Shapira, M.; Fernie, A.R.; Aharoni, A. Orchestration of thiamin biosynthesis and central metabolism by combined action of the thiamin pyrophosphate riboswitch and the circadian clock in arabidopsis. Plant Cell. 2013, 25, 288–307, doi:10.1105/tpc.112.106385.
[67]
Rapala-Kozik, M.; Wolak, N.; Kujda, M.; Banas, A. The upregulation of thiamine (vitamin b1) biosynthesis in arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biol. 2012, doi:10.1186/1471-2229-12-2.
[68]
Zimmermann, P.; Hirsch-Hoffmann, M.; Hennig, L.; Gruissem, W. Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 2004, 136, 2621–2632, doi:10.1104/pp.104.046367.
[69]
Leister, D. Retrograde signalling in plants: From simple to complex scenarios. Front. Plant Sci 2012, doi:10.3389/fpls.2012.00135.
[70]
Estavillo, G.M.; Chan, K.X.; Phua, S.Y.; Pogson, B.J. Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast. Front. Plant Sci 2013, doi:10.3389/fpls.2012.00300.
[71]
Caldana, C.; Fernie, A.R.; Willmitzer, L.; Steinhauser, D. Unravelling retrograde signalling pathways: Finding candidate signalling molecules via metabolomics and systems biology driven approaches. Front. Plant Sci 2012, doi:10.3389/fpls.2012.00267.
[72]
Strand, A.; Asami, T.; Alonso, J.; Ecker, J.R.; Chory, J. Chloroplast to nucleus communication triggered by accumulation of mg-protoporphyrinix. Nature 2003, 421, 79–83, doi:10.1038/nature01204.
[73]
Estavillo, G.M.; Crisp, P.A.; Pornsiriwong, W.; Wirtz, M.; Collinge, D.; Carrie, C.; Giraud, E.; Whelan, J.; David, P.; Javot, H.; et al. Evidence for a sal1-pap chloroplast retrograde pathway that functions in drought and high light signaling in arabidopsis. Plant Cell. 2011, 23, 3992–4012, doi:10.1105/tpc.111.091033.
[74]
Xiao, Y.; Savchenko, T.; Baidoo, E.; Chehab, W.; Hayden, D.; Tolstikov, V.; Corwin, J.; Kliebenstein, D.; Keasling, J.; Dehesh, K. Retrograde signaling by the plastidial metabolite mecpp regulates expression of nuclear stress-response genes. Cell. 2012, 149, 1525–1535, doi:10.1016/j.cell.2012.04.038.
[75]
Baruah, A.; ?imková, K.; Hincha, D.K.; Apel, K.; Laloi, C. Modulation of 1o2-mediated retrograde signaling by the pleiotropic response locus 1 (prl1) protein, a central integrator of stress and energy signaling. Plant J. 2009, 60, 22–32, doi:10.1111/j.1365-313X.2009.03935.x.
[76]
Ramel, F.; Birtic, S.; Ginies, C.; Soubigou-Taconnat, L.; Triantaphylides, C.; Havaux, M. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc. Natl. Acad. Sci. USA 2012, 109, 5535–5540.
[77]
Ankele, E.; Kindgren, P.; Pesquet, E.; Strand, ?. In vivo visualization of mg-protoporphyrinix, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell. 2007, 19, 1964–1979, doi:10.1105/tpc.106.048744.
[78]
Moulin, M.; McCormac, A.C.; Terry, M.J.; Smith, A.G. Tetrapyrrole profiling in arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to mg-protoporphyrin ix accumulation. Proc. Natl. Acad. Sci. USA 2008, 105, 15178–15183.
[79]
Mochizuki, N.; Tanaka, R.; Tanaka, A.; Masuda, T.; Nagatani, A. The steady-state level of mg-protoporphyrin ix is not a determinant of plastid-to-nucleus signaling in arabidopsis. Proc. Natl. Acad. Sci. USA 2008, 105, 15184–15189, doi:10.1073/pnas.0803245105.
[80]
Woodson, J.D.; Perez-Ruiz, J.M.; Chory, J. Heme synthesis by plastid ferrochelatase i regulates nuclear gene expression in plants. Curr. Biol. 2011, 21, 897–903, doi:10.1016/j.cub.2011.04.004.
[81]
Duncan, O.; Taylor, N.L.; Carrie, C.; Eubel, H.; Kubiszewski-Jakubiak, S.; Zhang, B.; Narsai, R.; Millar, A.H.; Whelan, J. Multiple lines of evidence localize signaling, morphology, and lipid biosynthesis machinery to the mitochondrial outer membrane of arabidopsis. Plant Physiol. 2011, 157, 1093–1113, doi:10.1104/pp.111.183160.
[82]
Duncan, O.; van der Merwe, M.J.; Daley, D.O.; Whelan, J. The outer mitochondrial membrane in higher plants. Trends Plant Sci. 2013, 18, 207–217, doi:10.1016/j.tplants.2012.12.004.
[83]
Giegé, P.; Heazlewood, J.L.; Roessner-Tunali, U.; Millar, A.H.; Fernie, A.R.; Leaver, C.J.; Sweetlove, L.J. Enzymes of glycolysis are functionally associated with the mitochondrion in arabidopsis cells. Plant Cell. 2003, 15, 2140–2151, doi:10.1105/tpc.012500.
[84]
Graham, J.W.A.; Williams, T.C.R.; Morgan, M.; Fernie, A.R.; Ratcliffe, R.G.; Sweetlove, L.J. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell. 2007, 19, 3723–3738, doi:10.1105/tpc.107.053371.
[85]
Cho, Y.-H.; Yoo, S.-D.; Sheen, J. Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell. 2006, 127, 579–589, doi:10.1016/j.cell.2006.09.028.
[86]
Moore, B.; Zhou, L.; Rolland, F.; Hall, Q.; Cheng, W.-H.; Liu, Y.-X.; Hwang, I.; Jones, T.; Sheen, J. Role of the arabidopsis glucose sensor hxk1 in nutrient, light, and hormonal signaling. Science 2003, 300, 332–336, doi:10.1126/science.1080585.
[87]
Cho, Y.-H.; Sheen, J.; Yoo, S.-D. Low glucose uncouples hexokinase1-dependent sugar signaling from stress and defense hormone abscisic acid and c2h4 responses in arabidopsis. Plant Physiol. 2010, 152, 1180–1182, doi:10.1104/pp.109.148957.
[88]
Kaplan, F.; Kopka, J.; Sung, D.Y.; Zhao, W.; Popp, M.; Porat, R.; Guy, C.L. 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. 2007, 50, 967–981, doi:10.1111/j.1365-313X.2007.03100.x.
[89]
Scheible, W.-R.; Morcuende, R.; Czechowski, T.; Fritz, C.; Osuna, D.; Palacios-Rojas, N.; Schindelasch, D.; Thimm, O.; Udvardi, M.K.; Stitt, M. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of arabidopsis in response to nitrogen. Plant Physiol. 2004, 136, 2483–2499, doi:10.1104/pp.104.047019.
[90]
Morcuende, R.; Bari, R.; Gibon, Y.; Zheng, W.; Pant, B.D.; Blaesing, O.; Usadel, B.; Czechowski, T.; Udvardi, M.K.; Stitt, M.; et al. Genome-wide reprogramming of metabolism and regulatory networks of arabidopsis in response to phosphorus. Plant Cell. Environ. 2007, 30, 85–112, doi:10.1111/j.1365-3040.2006.01608.x.
[91]
Armengaud, P.; Sulpice, R.; Miller, A.J.; Stitt, M.; Amtmann, A.; Gibon, Y. Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in arabidopsis roots. Plant Physiol. 2009, 150, 772–785, doi:10.1104/pp.108.133629.
[92]
Arroyo, A.; Bossi, F.; Finkelstein, R.R.; León, P. Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in arabidopsis. Plant Physiol. 2003, 133, 231–242, doi:10.1104/pp.103.021089.
[93]
Rizhsky, L.; Liang, H.; Shuman, J.; Shulaev, V.; Davletova, S.; Mittler, R. When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004, 134, 1683–1696, doi:10.1104/pp.103.033431.
[94]
Hummel, I.; Pantin, F.; Sulpice, R.; Piques, M.; Rolland, G.; Dauzat, M.; Christophe, A.; Pervent, M.; Bouteillé, M.; Stitt, M.; et al. Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: An integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol. 2010, 154, 357–372, doi:10.1104/pp.110.157008.
[95]
Van Houtte, H.; Vandesteene, L.; Lopez-Galvis, L.; Lemmens, L.; Kissel, E.; Carpentier, S.; Feil, R.; Avonce, N.; Beeckman, T.; Lunn, J.; et al. Over-expression of the trehalase gene attre1 leads to increased drought stress tolerance in arabidopsis and is involved in aba-induced stomatal closure. Plant Physiol. 2013, 161, 1158–1171, doi:10.1104/pp.112.211391.
[96]
Lippold, F.; Sanchez, D.H.; Musialak, M.; Schlereth, A.; Scheible, W.-R.; Hincha, D.K.; Udvardi, M.K. Atmyb41 regulates transcriptional and metabolic responses to osmotic stress in arabidopsis. Plant Physiol. 2009, 149, 1761–1772, doi:10.1104/pp.108.134874.
[97]
Baena-Gonzalez, E.; Rolland, F.; Thevelein, J.M.; Sheen, J. A central integrator of transcription networks in plant stress and energy signalling. Nature 2007, 448, 938–942, doi:10.1038/nature06069.
[98]
Jossier, M.; Bouly, J.-P.; Meimoun, P.; Arjmand, A.; Lessard, P.; Hawley, S.; Grahame Hardie, D.; Thomas, M. Snrk1 (snf1-related kinase 1) has a central role in sugar and aba signalling in Arabidopsis thaliana. Plant J. 2009, 59, 316–328, doi:10.1111/j.1365-313X.2009.03871.x.
[99]
Toroser, D.; Plaut, Z.; Huber, S.C. Regulation of a plant snf1-related protein kinase by glucose-6-phosphate. Plant Physiol. 2000, 123, 403–412, doi:10.1104/pp.123.1.403.
[100]
Zhang, Y.; Primavesi, L.F.; Jhurreea, D.; Andralojc, P.J.; Mitchell, R.A.C.; Powers, S.J.; Schluepmann, H.; Delatte, T.; Wingler, A.; Paul, M.J. Inhibition of snf1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 2009, 149, 1860–1871, doi:10.1104/pp.108.133934.
[101]
Paul, M.J.; Jhurreea, D.; Zhang, Y.; Primavesi, L.F.; Delatte, T.; Schluepmann, H.; Wingler, A. Up-regulation of biosynthetic processes associated with growth by trehalose 6-phosphate. Plant Signal. Behav 2010, 5, 386–392, doi:10.4161/psb.5.4.10792.
[102]
Fragoso, S.; Espíndola, L.; Páez-Valencia, J.; Gamboa, A.; Camacho, Y.; Martínez-Barajas, E.; Coello, P. Snrk1 isoforms akin10 and akin11 are differentially regulated in arabidopsis plants under phosphate starvation. Plant Physiol. 2009, 149, 1906–1916.
[103]
Kolbe, A.; Tiessen, A.; Schluepmann, H.; Paul, M.; Ulrich, S.; Geigenberger, P. Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of adp-glucose pyrophosphorylase. Proc. Natl. Acad. Sci. USA 2005, 102, 11118–11123, doi:10.1073/pnas.0503410102.
[104]
Delatte, T.L.; Sedijani, P.; Kondou, Y.; Matsui, M.; de Jong, G.J.; Somsen, G.W.; Wiese-Klinkenberg, A.; Primavesi, L.F.; Paul, M.J.; Schluepmann, H. Growth arrest by trehalose-6-phosphate: An astonishing case of primary metabolite control over growth by way of the snrk1 signaling pathway. Plant Physiol. 2011, 157, 160–174, doi:10.1104/pp.111.180422.
[105]
Rahmani, F.; Hummel, M.; Schuurmans, J.; Wiese-Klinkenberg, A.; Smeekens, S.; Hanson, J. Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiol. 2009, 150, 1356–1367, doi:10.1104/pp.109.136036.
[106]
Wahl, V.; Ponnu, J.; Schlereth, A.; Arrivault, S.; Langenecker, T.; Franke, A.; Feil, R.; Lunn, J.E.; Stitt, M.; Schmid, M. Regulation of flowering by trehalose-6-phosphate signaling in arabidopsis thaliana. Science 2013, 339, 704–707, doi:10.1126/science.1230406.
[107]
Cho, Y.-H.; Hong, J.-W.; Kim, E.-C.; Yoo, S.-D. Regulatory functions of snrk1 in stress-responsive gene expression and in plant growth and development. Plant Physiol. 2012, 158, 1955–1964, doi:10.1104/pp.111.189829.
[108]
Ng, S.; Giraud, E.; Duncan, O.; Law, S.R.; Wang, Y.; Xu, L.; Narsai, R.; Carrie, C.; Walker, H.; Day, D.A.; et al. Cyclin-dependent kinase e1 (cdke1) provides a cellular switch in plants between growth and stress responses. J. Biol. Chem. 2013, 288, 3449–3459, doi:10.1074/jbc.M112.416727.
[109]
Nargang, F.E.; Adames, K.; Rüb, C.; Cheung, S.; Easton, N.; Nargang, C.E.; Chae, M.S. Identification of genes required for alternative oxidase production in the neurospora crassa gene knockout library. G3 (Bethesda) 2012, 2, 1345–1356, doi:10.1534/g3.112.004218.
[110]
Giraud, E.; Van Aken, O.; Ho, L.H.M.; Whelan, J. The transcription factor abi4 is a regulator of mitochondrial retrograde expression of alternative oxidase1a. Plant Physiol. 2009, 150, 1286–1296, doi:10.1104/pp.109.139782.
[111]
Koussevitzky, S.; Nott, A.; Mockler, T.C.; Hong, F.; Sachetto-Martins, G.; Surpin, M.; Lim, J.; Mittler, R.; Chory, J. Signals from chloroplasts converge to regulate nuclear gene expression. Science 2007, 316, 715–719, doi:10.1126/science.1140516.
[112]
Giraud, E.; Ho, L.H.M.; Clifton, R.; Carroll, A.; Estavillo, G.; Tan, Y.-F.; Howell, K.A.; Ivanova, A.; Pogson, B.J.; Millar, A.H.; et al. The absence of alternative oxidase1a in arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 2008, 147, 595–610, doi:10.1104/pp.107.115121.
[113]
Shkolnik-Inbar, D.; Adler, G.; Bar-Zvi, D. Abi4 downregulates expression of the sodium transporter hkt1;1 in arabidopsis roots and affects salt tolerance. Plant J. 2013, 73, 993–1005, doi:10.1111/tpj.12091.
[114]
Van Aken, O.; Whelan, J. Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in arabidopsis. Front. Plant Sci 2012, doi:10.3389/fpls.2012.00267.
[115]
Cho, Y.-H.; Yoo, S.-D. Signaling role of fructose mediated by fins1/fbp in arabidopsis thaliana. PLoS Genet. 2011, 7, e1001263, doi:10.1371/journal.pgen.1001263.
[116]
Ko?mann, J.; Sonnewald, U.; Willmitzer, L. Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J. 1994, 6, 637–650.
[117]
Zrenner, R.; Krause, K.-P.; Apel, P.; Sonnewald, U. Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J. 1996, 9, 671–681.
[118]
Arsova, B.; Hoja, U.; Wimmelbacher, M.; Greiner, E.; üstün, ?.; Melzer, M.; Petersen, K.; Lein, W.; B?rnke, F. Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: Evidence for an essential role in chloroplast development in arabidopsis and nicotiana benthamiana. Plant Cell. 2010, 22, 1498–1515, doi:10.1105/tpc.109.071001.
[119]
Deprost, D.; Yao, L.; Sormani, R.; Moreau, M.; Leterreux, G.; Nicolai, M.; Bedu, M.; Robaglia, C.; Meyer, C. The arabidopsis tor kinase links plant growth, yield, stress resistance and mrna translation. EMBO Rep. 2007, 8, 864–870, doi:10.1038/sj.embor.7401043.
[120]
Mahfouz, M.M.; Kim, S.; Delauney, A.J.; Verma, D.P.S. Arabidopsis target of rapamycin interacts with raptor, which regulates the activity of s6 kinase in response to osmotic stress signals. Plant Cell. 2006, 18, 477–490, doi:10.1105/tpc.105.035931.
[121]
Moreau, M.; Azzopardi, M.; Clément, G.; Dobrenel, T.; Marchive, C.; Renne, C.; Martin-Magniette, M.-L.; Taconnat, L.; Renou, J.-P.; Robaglia, C.; et al. Mutations in the arabidopsis homolog of lst8/gβl, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell. 2012, 24, 463–481, doi:10.1105/tpc.111.091306.
[122]
Jazwinski, S.M. The retrograde response: When mitochondrial quality control is not enough. Biochim. Biophys. Acta 2013, 1833, 400–409, doi:10.1016/j.bbamcr.2012.02.010.
[123]
Warren, C.; Aranda, I.; Cano, F.J. Metabolomics demonstrates divergent responses of two eucalyptus species to water stress. Metabolomics 2012, 8, 186–200, doi:10.1007/s11306-011-0299-y.
[124]
Yobi, A.; Wone, B.W.M.; Xu, W.; Alexander, D.C.; Guo, L.; Ryals, J.A.; Oliver, M.J.; Cushman, J.C. Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of selaginella reveals insights into the resurrection trait. Plant J. 2012, 72, 983–999.
[125]
Sanchez, D.H.; Pieckenstain, F.L.; Szymanski, J.; Erban, A.; Bromke, M.; Hannah, M.A.; Kraemer, U.; Kopka, J.; Udvardi, M.K. Comparative functional genomics of salt stress in related model and cultivated plants identifies and overcomes limitations to translational genomics. PLoS One 2011, 6, e17094, doi:10.1371/journal.pone.0017094.
[126]
Sanchez, D.H.; Schwabe, F.; Erban, A.; Udvardi, M.K.; Kopka, J. Comparative metabolomics of drought acclimation in model and forage legumes. Plant Cell. Environ. 2012, 35, 136–149, doi:10.1111/j.1365-3040.2011.02423.x.
[127]
Widodo; Patterson, J.H.; Newbigin, E.; Tester, M.; Bacic, A.; Roessner, U. Metabolic responses to salt stress of barley (hordeum vulgare l.) cultivars, sahara and clipper, which differ in salinity tolerance. J. Exp. Bot. 2009, 60, 4089–4103, doi:10.1093/jxb/erp243.
Stitt, M.; Sulpice, R.; Keurentjes, J. Metabolic networks: How to identify key components in the regulation of metabolism and growth. Plant Physiol. 2010, 152, 428–444, doi:10.1104/pp.109.150821.
[130]
Riedelsheimer, C.; Lisec, J.; Czedik-Eysenberg, A.; Sulpice, R.; Flis, A.; Grieder, C.; Altmann, T.; Stitt, M.; Willmitzer, L.; Melchinger, A.E. Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 8872–8877, doi:10.1073/pnas.1120813109.
[131]
Sulpice, R.; Nikoloski, Z.; Tschoep, H.; Antonio, C.; Kleessen, S.; Larhlimi, A.; Selbig, J.; Ishihara, H.; Gibon, Y.; Fernie, A.R.; et al. Impact of the carbon and nitrogen supply on relationships and connectivity between metabolism and biomass in a broad panel of arabidopsis accessions. Plant Physiol. 2013, 162, 347–363, doi:10.1104/pp.112.210104.
[132]
Degenkolbe, T.; Giavalisco, P.; Zuther, E.; Seiwert, B.; Hincha, D.K.; Willmitzer, L. Differential remodeling of the lipidome during cold acclimation in natural accessions of arabidopsis thaliana. Plant J. 2012, 72, 972–982.
[133]
Lindsley, J.E.; Rutter, J. Whence cometh the allosterome? Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 10533–10535, doi:10.1073/pnas.0604452103.
[134]
Fernie, A.R.; Morgan, J.A. Analysis of metabolic flux using dynamic labelling and metabolic modelling. Plant Cell. Environ. 2013, 36, 1738–1750, doi:10.1111/pce.12083.
[135]
Baxter, C.; Redestig, H.; Schauer, N.; Repsilber, D.; Patil, K.; Nielsen, J.; Selbig, J.; Liu, J.; Fernie, A.; Sweetlove, L. The metabolic response of heterotrophic arabidopsis cells to oxidative stress. Plant Physiol. 2007, 143, 312–325.
[136]
Lehmann, M.; Laxa, M.; Sweetlove, L.; Fernie, A.; Obata, T. Metabolic recovery of arabidopsis thaliana roots following cessation of oxidative stress. Metabolomics 2012, 8, 143–153, doi:10.1007/s11306-011-0296-1.
[137]
Giavalisco, P.; Ko?hl, K.; Hummel, J.; Seiwert, B.; Willmitzer, L. 13c isotope-labeled metabolomes allowing for improved compound annotation and relative quantification in liquid chromatography-mass spectrometry-based metabolomic research. Anal. Chem. 2009, 81, 6546–6551, doi:10.1021/ac900979e.
[138]
Nakabayashi, R.; Saito, K. Metabolomics for unknown plant metabolites. Anal. Bioanal Chem 2013, 405, 5005–5011, doi:10.1007/s00216-013-6869-2.
[139]
Nakabayashi, R.; Sawada, Y.; Yamada, Y.; Suzuki, M.; Hirai, M.Y.; Sakurai, T.; Saito, K. Combination of liquid chromatography–fourier transform ion cyclotron resonance-mass spectrometry with 13c-labeling for chemical assignment of sulfur-containing metabolites in onion bulbs. Anal. Chem. 2013, 85, 1310–1315, doi:10.1021/ac302733c.
[140]
Bocobza, S.E.; Willmitzer, L.; Raikhel, N.; Aharoni, A. Discovery of new modules in metabolic biology using chemometabolomics. Plant Physiol. 2012, 160, 1160–1163, doi:10.1104/pp.112.203919.
[141]
Tohge, T.; Ramos, M.S.; Nunes-Nesi, A.; Mutwil, M.; Giavalisco, P.; Steinhauser, D.; Schellenberg, M.; Willmitzer, L.; Persson, S.; Martinoia, E.; et al. Toward the storage metabolome: Profiling the barley vacuole. Plant Physiol. 2011, 157, 1469–1482, doi:10.1104/pp.111.185710.
[142]
Moussaieff, A.; Rogachev, I.; Brodsky, L.; Malitsky, S.; Toal, T.W.; Belcher, H.; Yativ, M.; Brady, S.M.; Benfey, P.N.; Aharoni, A. High-resolution metabolic mapping of cell types in plant roots. Proc. Natl. Acad. Sci. USA 2013, 110, E1232–E1241, doi:10.1073/pnas.1302019110.
[143]
Long, T.A.; Tsukagoshi, H.; Busch, W.; Lahner, B.; Salt, D.E.; Benfey, P.N. The bhlh transcription factor popeye regulates response to iron deficiency in arabidopsis roots. Plant Cell. 2010, 22, 2219–2236, doi:10.1105/tpc.110.074096.