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
© Rapala-Kozik et al; licensee BioMed Central Ltd. 2011
Received: 11 September 2011
Accepted: 3 January 2012
Published: 3 January 2012
Recent reports suggest that vitamin B1 (thiamine) participates in the processes underlying plant adaptations to certain types of abiotic and biotic stress, mainly oxidative stress. Most of the genes coding for enzymes involved in thiamine biosynthesis in Arabidopsis thaliana have been identified. In our present study, we examined the expression of thiamine biosynthetic genes, of genes encoding thiamine diphosphate-dependent enzymes and the levels of thiamine compounds during the early (sensing) and late (adaptation) responses of Arabidopsis seedlings to oxidative, salinity and osmotic stress. The possible roles of plant hormones in the regulation of the thiamine contribution to stress responses were also explored.
The expression of Arabidopsis genes involved in the thiamine diphosphate biosynthesis pathway, including that of THI1, THIC, TH1 and TPK, was analyzed for 48 h in seedlings subjected to NaCl or sorbitol treatment. These genes were found to be predominantly up-regulated in the early phase (2-6 h) of the stress response. The changes in these gene transcript levels were further found to correlate with increases in thiamine and its diphosphate ester content in seedlings, as well as with the enhancement of gene expression for enzymes which require thiamine diphosphate as a cofactor, mainly α-ketoglutarate dehydrogenase, pyruvate dehydrogenase and transketolase. In the case of the phytohormones including the salicylic, jasmonic and abscisic acids which are known to be involved in plant stress responses, only abscisic acid was found to significantly influence the expression of thiamine biosynthetic genes, the thiamine diphosphate levels, as well as the expression of genes coding for main thiamine diphosphate-dependent enzymes. Using Arabidopsis mutant plants defective in abscisic acid production, we demonstrate that this phytohormone is important in the regulation of THI1 and THIC gene expression during salt stress but that the regulatory mechanisms underlying the osmotic stress response are more complex.
On the basis of the obtained results and earlier reported data, a general model is proposed for the involvement of the biosynthesis of thiamine compounds and thiamine diphosphate-dependent enzymes in abiotic stress sensing and adaptation processes in plants. A possible regulatory role of abscisic acid in the stress sensing phase is also suggested by these data.
Two further thiamine biosynthetic steps include an additional phosphorylation of HMP-P to 4-amino-2-methyl-5-hydroxymethylpyrimidine diphosphate (HMP-PP) and the condensation of HMP-PP with HET-P to form thiamine monophosphate (TMP). These two reactions are catalyzed by a single protein, the product of the TH1 gene in Arabidopsis  or THI3 gene in Z. mays , which is thus a bifunctional enzyme with both HMP-P kinase and TMP synthase activities. TMP does not possess any recognized physiological function to date but constitutes a thiamine resource or transitional stage for further TDP synthesis. In the latter case, an unphosphorylated form of thiamine is required. As has been shown previously in Z. mays , TMP is dephosphorylated by a relatively unspecific phosphatase which can also use TDP as a substrate. All of the steps described above proceed in chloroplasts , but the process of thiamine conversion to TDP occurs in the cytosol and is catalyzed by thiamine pyrophosphokinase, encoded by the TPK genes . To fulfill its biological function, TDP must be transported to chloroplasts or mitochondria but the required transporters have not yet been identified. The thiamine biosynthesis pathway in plants is precisely regulated through TDP-dependent riboswitch mechanisms on the THIC gene and in ancient plant taxa also the THI1 gene levels .
It has been well documented that thiamine biosynthesis is activated during plant adaptation responses to persistent abiotic stress conditions such as salting and flooding , cold, heat and drought [17, 18], and oxidative stress [19, 20]. However, it has not yet been determined how thiamine biosynthesis and activation responds to the above stimuli at the early stages of the corresponding stress responses (sensing). In our current study, we further characterize the role of thiamine biosynthesis upregulation in the early response to oxidative, osmotic and salt stress in plants. In the experiments, we analyze changes in the expression levels of all thiamine-biosynthetic genes and of genes encoding the major TDP-dependent enzymes such as TK, KGDH, PDH, PDC and DXPS in Arabidopsis seedlings. We also show for the first time that abscisic acid (ABA), but not salicylic acid (SA), is involved in the upregulation of thiamine biosynthesis in the plant response to abiotic stress.
Increased expression of thiamine biosynthesis genes during early response of Arabidopsis seedlings to oxidative, salt and osmotic stress
Early response of TDP-dependent enzymes to oxidative, salt and osmotic stress
Involvement of plant hormones in the up-regulation of thiamine biosynthesis during early response to stress
Because their growth and development are affected by environmental fluctuations, plants require fast responses to these changes for the maintenance of internal homeostasis. Hence, a number of sensitive mechanisms have evolved in plants to allow rapid sensing of environmental cues and facilitate growth modifications for adaptation and survival [21, 22]. As stress has an impact on the carbon fixation and overall energy status of plants, most previous genetic, proteomic and metabolic studies of this area have dealt with changes in glycolysis, the tricarboxylic acid cycle, the pentose phosphate pathway and photosynthesis [23–25]. However, these earlier reports have presented data that was obtained under very different growth or stress conditions, and also over quite different time scales and using different measurement parameter. This makes it difficult to compare the results from different laboratories in a meaningful way.
In our current study, which for the first time evaluates the early response stage ("stress sensing") rather than the long-term adaptation to stress in plants, we compared (i) the expression levels of the genes involved in thiamine/TDP biosynthesis pathways; (ii) the expression levels of genes coding for the most important TDP-requiring enzymes; and (iii) the thiamine and its phosphate ester contents, in Arabidopsis seedlings treated with abiotic stressors including PQ, NaCl and SOR. The application of NaCl or SOR into the plant growth media during the first few hours of treatment is sensed by the plants as general water stress rather than as salt- or SOR-specific effects . It is generally accepted, that stress-generated damage involves the most important pathways and hence an obvious need to upregulate the main biosynthetic processes, including the biosynthesis of TDP. Indeed, we observed in our present experiments that the expression of all TDP-biosynthesis genes had already been increased at 2 h after the application of two water-stress agents (Figure 2). Interestingly, these genes showed decreased expression under salt stress over a longer time scale of several days, suggesting an extensive ion penetration into plant tissues  that could possibly generate new stimuli and adaptation processes. However, in our SOR stress experiments, the most of the early observed changes, particularly those involving the THIC gene, were maintained over a long time scale. This may indicate that a hormonal signaling mechanism rather than water availability controls plant growth under these conditions . Surprisingly, we did not observe any marked influence of PQ on the expression of TDP biosynthesis genes over a time scale of a few hours, which is in contrast to the findings of an earlier study of long-lasting PQ-generated oxidative stress .
Our observed increases in gene expression during initial stages of the plant stress responses may indicate that (i) the translated proteins are susceptible to damage under unfavorable conditions and an increase of transcription is therefore required to maintain the proper thiamine cellular levels; (ii) the TDP-dependent enzymes are destroyed and, parallel to their re-synthesis, a new requirement for their cofactors emerges; and/or (iii) thiamine production is necessary to overcome the consequences of stress or to develop new adaptation strategies. Our analysis of thiamine and its phosphate analogs in stressed plants (Figure 3) showed that the observed changes in the expression of thiamine biosynthetic genes correlated with the activity of the encoded enzymes. The increase in the thiamine and TDP contents during the early Arabidopsis response (sensing) to water stress is consistent with similar changes recently reported in Z. mays seedlings subjected to long-lasting osmotic, oxidative and salinity stress . This suggests that during stress sensing and adaptation in plants, the biosynthesis of thiamine is tightly regulated. Moreover, this regulation does not seem to be specific to the type of stress and could benefit from two different mechanisms previously identified in plants. The first type of possible regulation occurs at the genetic level and can apply to the THIC gene promoter as it contains a TDP-dependent riboswitch . The other regulation process can operate at the protein level, as was demonstrated in a study of Z. mays, where TMP synthase activity was strongly inhibited by an increased supply of HMP-PP, produced through the activity of the kinase domain of the same protein, THI3 .
To test the hypothesis that the effects of stress conditions on thiamine compound pools in plant tissues arise from the increased requirement for TDP from the TDP-dependent main catabolic pathways, we analyzed the stress-dependent changes in the expression of several genes encoding TDP-dependent enzymes (Figure 4). The mitochondrial production of acetyl CoA and the tricarboxylic acid cycle are assumed to be the first plant sensors of oxidative stress [23, 28, 29]. Our current analyses identified KGDH and PDH as the main source of stress perturbation. However, the upregulation of the expression of these two mitochondrial TDP-dependent enzymes can result not only from the increased requirement for mitochondrial potential restoration, respiration control, nitrogen metabolism or glutamate signaling  but also reflect the activation of a stress signaling response to a metabolic imbalance as a result of a KGDH side reaction resulting in reactive oxygen species production .
The TK enzyme, which operates in the chloroplastic Calvin-Benson cycle (CBC), is involved in carbon fixation  and its activity is a limiting factor for sucrose production and photosynthesis . As it functions also in the pentose phosphate pathway, TK is additionally important for the generation of NADPH, cooperating with a variety of oxidant-scavenging systems [23, 33–35]. The early reported increase in TK transcripts in Arabidopsis agrees with the changes in TK activity observed in Z. mays under salt and oxidative stress  and supports the hypothesis that this enzyme is involved in plant stress protection. DXPS is another TDP-dependent enzyme which is involved in the production of powerful antioxidants, the carotenoids [36, 37]. The activation of carotenoid synthetic pathways has been observed during osmotic, salt and drought stress [38–40]. In our present study, however, no significant changes in the expression of DXPS-encoding gene were observed over 24 h of stress treatment, possibly because its regulation occurs at the posttranscriptional level .
The well characterized and essential roles of the phytohormones in a wide range of stress adaptive processes in plants [42, 43] prompted us to search for candidate regulators of the activation of thiamine biosynthesis and TDP-dependent metabolic processes during salt and osmotic stress sensing and in the later adaptation phase. Our focus on SA was based on previous reports of an activation of a cabbage THIJ-like gene product involved in HMP phosphorylation via the SA-dependent signaling pathway  and an involvement of SA in thiamine-induced plant resistance to pathogen attacks . However, our treatments of Arabidopsis plants with exogenous SA did not cause any observable changes in expression of genes involved in thiamine biosynthesis (Figures 5 and 6).
JA is associated with the defense against necrotrophic pathogens and herbivorous insects  but its involvement in salt stress-dependent gene regulation has also been suggested . In our current study, supplementation of growth medium with JA caused a slightly increased thiamine content in Arabidopsis seedlings, resulting from the activation of thiamine biosynthetic genes, mostly TH1 (Figures 5 and 6). Although the mechanism underlying thiamine biosynthesis regulation by JA requires further analysis, it is noteworthy that a cis-acting element T/GBOXATPIN2 (AACGTG) was identified in the TH1 promoter region  which is responsible for activating this gene in response to JA upon wounding .
ABA regulates nearly 10% of the protein-coding genes in plants  and commonly participates in the transcriptional regulation processes that operate under salt and osmotic stress conditions [51–54]. The upregulation of the THI1, THIC, TH1 and TPK genes and the 3.5-fold increase in the total thiamine levels in Arabidopsis seedlings under the influence of an external ABA supply that we observed in this study provide the first evidence for the involvement of ABA in thiamine biosynthesis under stress conditions (Figures 5, 6). These findings are also interpretable in the light of previous analyses of THI1and THIC promoters that showed the presence of an ABA-responsive element (ABRE) in the THI1 promoter  and putative stress-related elements in the THIC promoter, including ABRE and drought-response element . In silico analysis of the TPK promoter has identified a dehydration and ABA-inducible expression element MYBATRD22 (CTAACCA) and of the TH1 promoter an ABRE - ABRELATERD1 (ACGTG) element.
Our current analysis of the expression of TDP-dependent enzymes in seedlings grown on ABA-containing medium showed a transcript accumulation for KGDH- and TK-encoding genes but no significant effects on PDH gene transcripts. These data are consistent with our previous observations of the increased ABA content and TK activity in Z. mays seedlings treated with NaCl and polyethylene glycol . Taken together, these data are consistent with the well established hypothesis regarding the linkages between ABA and plant mitochondrial functionality [55–57].
Although the application of exogenous ABA has often been used to mimic water stress responses in plants , it is generally accepted that both ABA-dependent and ABA-independent processes are involved in these types of responses . In an attempt to further validate the hypothesis that ABA is responsible for thiamine biosynthesis in the early response (sensing) of plants to water stress generated by salt or SOR, a mutant Arabidopsis plant (aba1) was employed in our present experiments. This mutant is defective in the production of zeaxanthin epoxidase, an enzyme that catalyzes two early steps in the generation of the epoxycarotenoid precursor as part of the ABA biosynthetic pathway . In the analysis, aba1 showed different behaviors in response to salt and osmotic stress. Under salt stress, a decrease in the THI1 and THIC expression levels in the aba1 mutant plants was observed, confirming the regulation of these thiamine biosynthetic steps by ABA. The expression of TH1 and TPK was found to be maintained as in the wild type plant. In contrast, in the presence of SOR the activation of thiamine biosynthetic genes was found not to be markedly different from wild type plants, suggesting that some additional, e.g. post-transcriptional, regulatory processes for thiamine biosynthesis operate under these conditions, although the details remain to be clarified.
Our present findings suggest a contribution of ABA to the transcriptional regulation of the two first genes that function in thiamine biosynthesis (THI1 and THIC) in Arabidopsis seedlings subjected to salt and osmotic stress, particularly at the early stages of the stress response (i.e. stress sensing). However, other as yet unidentified endogenous mediators must also be involved and the relative importance of ABA becomes less significant over a longer time scale (i.e. during the plant adaptation to stress). Moreover, the TH1 and TPK genes appear to be regulated by endogenous factors other than ABA, but also by ABA when it is present in the growth medium.
We here demonstrate for the first time that TDP biosynthesis processes are quickly activated during the early phase (sensing) of the Arabidopsis response to salt and osmotic stress. The produced TDP is incorporated into TDP-dependent enzymes that are up-regulated at the same time such as KGDH, PDH, TK, all of which are involved in the main metabolic pathways that respond to stress conditions in plants. ABA seems to be involved in the activation of genes encoding enzymes that function in thiamine and TDP biosynthesis as well as the TDP-dependent KGDH and TK genes. We propose a working model for the contribution of thiamine to the stress sensing and adaptation processes in plants.
Materials and methods
Plant materials, growth conditions and stress treatments
The seeds of Arabidopsis thaliana ecotype Columbia (Lehle, Round Rock, TX, USA) were used for all gene expression analysis performed for the detection of thiamine biosynthesis and activation processes. The seeds of the ABA-deficient mutant aba1 (CS21) were obtained from the Arabidopsis Biological Resource Center (ABRC, Columbus, OH, USA). For comparative analyses using this mutant, wild-type Arabidopsis plants of the background ecotype Landsberg erecta were used.
Arabidopsis seeds (100 mg) were surface sterilized by treatment for 5 min with 0.5% Tween-20, for 5 min with 70% ethanol and for 7 min with a 15% bleach solution. Water-rinsed seeds were stratified for three days at 4°C and then grown on Murashige and Skoog (MS) agar plates supplemented with 1% sucrose but depleted of thiamine, under a 12 h light/12 h dark cycle at 22°C, with a constant light intensity of 100 μmol m-2 s-1. Nine-day old seedlings were then transferred and grown for 2-48 h on MS media containing 0.2 μM PQ, 200 mM NaCl, 200 mM SOR, 100 μM ABA, 100 μM JA or 200 μM SA. All experiments were performed with 3-5 replicates of 20 seedlings per treatment.
RNA isolation and quantitative real-time PCR
The list of analyzed genes and selected PCR primers used in real-time PCR.
Forward primer (FP)Reverse primer (RP)
Tm FP or RP(°C)
HPLC analysis of thiamine and its phosphate analogs
Assays of thiamine and its phosphate analogs in Arabidopsis seedlings were carried out using a previously described method . Briefly, plant extracts were prepared by 12% TCA treatment of frozen, ground Arabidopsis seedlings for 5 min at 4°C. After removal of the protein pellet and TCA disposal by ethyl ether treatment, the supernatant was analyzed by reverse-phase high performance liquid chromatography (RP-HPLC) with post-column oxidation using 90 μM sodium hexacyanoferrate (III) in 0.56 M NaOH and fluorescence detection of the formed thiochrome and thiochrome phosphates . For RP-HPLC separation, gradient elution (0-90%B, 16 min) was used, where solvent A contained 15 mM ammonium citrate (pH 4.2) and solvent B consisted of 0.1 M formic acid and 55 mM diethylamine. The applied HPLC equipment contained a Shimadzu (Kyoto, Japan) model LC-9A HPLC pump with Shimadzu FCV-AL proportioning valve, a Knauer (Bad Homburg, Germany) model A0263 manual injector, a Merck cartridge LiChrosphere 100RP-18 column (250 × 3.4 mm), a Shimadzu model RF-535 fluorescence monitor (excitation at 365 nm, emission at 430 nm) and Shimadzu Class-VP software (version 4) for pump control, data acquisition and analysis.
The authors thank Professor Andrzej Kozik for helpful discussions and critical reading of the manuscript. This work was supported in part by the Polish Ministry of Science and Higher Education (the grant No. NN303 320937 to M. R-K) and by Jagiellonian University (statutory funds No. DS15/WBBiB).
- Frank RA, Leeper FJ, Luisi BF: Structure, mechanism and catalytic duality of thiamine-dependent enzymes. Cell Mol Life Sci. 2007, 64: 892-905. 10.1007/s00018-007-6423-5.PubMedView ArticleGoogle Scholar
- Jurgenson CT, Begley TP, Ealick SE: The structural and biochemical foundations of thiamin biosynthesis. Ann Rev Biochem. 2009, 78: 569-603. 10.1146/annurev.biochem.78.072407.102340.PubMedView ArticleGoogle Scholar
- Kowalska E, Kozik A: The genes and enzymes involved in the biosynthesis of thiamin and thiamin diphosphate in yeasts. Cell Mol Biol Lett. 2008, 13: 271-282. 10.2478/s11658-007-0055-5.PubMedView ArticleGoogle Scholar
- Goyer A: Thiamine in plants: aspects of its metabolism and functions. Phytochemistry. 2010, 71: 1615-1624. 10.1016/j.phytochem.2010.06.022.PubMedView ArticleGoogle Scholar
- Rapala-Kozik M: Vitamine B1 (thiamine): a cofactor for enzymes involved in the main metabolic pathways and an environmental stress protectant. Adv Bot Res. 2011, 58: 37-90.View ArticleGoogle Scholar
- Raschke M, Burkle L, Muller N, Nunes-Nesi A, Fernie AR, Arigoni D, Amrhein N, Fitzpatrick TB: Vitamin B1 biosynthesis in plants requires the essential iron sulfur cluster protein, THIC. Proc Natl Acad Sci USA. 2007, 104: 19637-19642. 10.1073/pnas.0709597104.PubMedPubMed CentralView ArticleGoogle Scholar
- Chatterjee A, Schroeder FC, Jurgenson CT, Ealick SE, Begley TP: Biosynthesis of the thiamin-thiazole in eukaryotes: identification of a thiazole tautomer intermediate. J Am Chel Soc. 2008, 130: 1394-11398.Google Scholar
- Machado CR, de Oliveira RL, Boiteux S, Praekelt UM, Meacock PA, Menck CF: Thi1, a thiamine biosynthetic gene in Arabidopsis thaliana, complements bacterial defects in DNA repair. Plant Mol Biol. 1996, 31: 585-593. 10.1007/BF00042231.PubMedView ArticleGoogle Scholar
- Belanger F, Leustek T, Chu B, Kirz A: Evidence for the thiamine biosynthetic pathway in higher plant plastids and its developmental regulation. Plant Mol Biol. 1995, 29: 809-821. 10.1007/BF00041170.PubMedView ArticleGoogle Scholar
- Ajjawi I, Tsegaye Y, Shintani D: Determination of the genetic, molecular, and biochemical basis of the Arabidopsis thaliana thiamin auxotroph th1. Arch Biochem Biophys. 2007, 459: 107-114. 10.1016/j.abb.2006.11.011.PubMedView ArticleGoogle Scholar
- Rapala-Kozik M, Olczak M, Ostrowska K, Starosta A, Kozik A: Molecular characterization of the thi3 gene involved in thiamine biosynthesis in Zea mays: cDNA sequence and enzymatic and structural properties of the recombinant bifunctional protein with 4-amino-5-hydroxymethyl-2-methylpyrimidine (phosphate) kinase and thiamine monophosphate synthase activities. Biochem J. 2007, 408: 149-159. 10.1042/BJ20070677.PubMedPubMed CentralView ArticleGoogle Scholar
- Rapala-Kozik M, Golda A, Kujda M: Enzymes that control the thiamine diphosphate pool in plant tissues. Properties of thiamine pyrophosphokinase and thiamine-(di)phosphate phosphatase purified from Zea mays seedlings. Plant Physiol Biochem. 2009, 47: 237-242. 10.1016/j.plaphy.2008.12.015.PubMedView ArticleGoogle Scholar
- Julliard JH, Douce R: Biosynthesis of the thiazole moiety of thiamin (vitamin B1) in higher plant chloroplasts. P Natl Acad Sci USA. 1991, 88: 2042-2045. 10.1073/pnas.88.6.2042.View ArticleGoogle Scholar
- Ajjawi I, Rodriguez Milla MA, Cushman J, Shintani DK: Thiamin pyrophosphokinase is required for thiamin cofactor activation in Arabidopsis. Plant Mol Biol. 2007, 65: 151-162. 10.1007/s11103-007-9205-4.PubMedView ArticleGoogle Scholar
- Bocobza S, Aharoni A: Switching the light on plant riboswitches. Trends Plant Sci. 2008, 13: 526-533. 10.1016/j.tplants.2008.07.004.PubMedView ArticleGoogle Scholar
- Ribeiro DT, Farias LP, de Almeida JD, Kashiwabara PM, Ribeiro AF, Silva-Filho MC, Menck CF, Van Sluys MA: Functional characterization of the thi1 promoter region from Arabidopsis thaliana. J Exp Bot. 2005, 56: 1797-1804. 10.1093/jxb/eri168.PubMedView ArticleGoogle Scholar
- Ferreira S, Hjerno K, Larsen M, Wingsle G, Larsen P, Fey S, Roepstorff P, Salome Pais M: Proteome profiling of Populus euphratica Oliv. upon heat stress. Ann Bot. 2006, 98: 361-377. 10.1093/aob/mcl106.PubMedPubMed CentralView ArticleGoogle Scholar
- Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA: Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol. 2006, 140: 1437-1450. 10.1104/pp.105.070508.PubMedPubMed CentralView ArticleGoogle Scholar
- Rapala-Kozik M, Kowalska E, Ostrowska K: Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J Exp Bot. 2008, 59: 4133-4143. 10.1093/jxb/ern253.PubMedView ArticleGoogle Scholar
- Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D: Thiamin confers enhanced tolerance to oxidativestress in Arabidopsis. Plant Physiol. 2009, 151: 421-432. 10.1104/pp.109.140046.PubMedPubMed CentralView ArticleGoogle Scholar
- Taylor NL, Tan Y-F, Jacoby RP, Millar AH: Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics. 2009, 72: 367-378. 10.1016/j.jprot.2008.11.006.PubMedView ArticleGoogle Scholar
- Baena-Gonzalez E: Energy signaling in the regulation of gene expression during stress. Mol Plant. 2010, 3: 300-313. 10.1093/mp/ssp113.PubMedView ArticleGoogle Scholar
- Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ: The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol. 2007, 143: 312-325.PubMedPubMed CentralView ArticleGoogle Scholar
- Williams TC, Poolman MG, Howden AJ, Schwarzlander M, Fell DA, Ratcliffe RG, Sweetlove LJ: A genome-scale metabolic model accurately predicts fluxes in central carbon metabolism under stress conditions. Plant Physiol. 2010, 154: 311-323. 10.1104/pp.110.158535.PubMedPubMed CentralView ArticleGoogle Scholar
- Obata T, Matthes A, Koszior S, Lehmann M, Araújo WL, Bock R, Sweetlove LJ, Fernie AR: Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry. 2011, 72: 1081-1091. 10.1016/j.phytochem.2010.11.003.PubMedView ArticleGoogle Scholar
- Munns R: Comparative physiology of salt and water stress. Plant Cell Einviron. 2002, 25: 239-250. 10.1046/j.0016-8025.2001.00808.x.View ArticleGoogle Scholar
- Munns R, Passioura JB, Guo J, Chazen O, Cramer GR: Water relations and leaf expansion: importance of time scale. J Exp Bot. 2000, 51: 1495-1504. 10.1093/jexbot/51.350.1495.PubMedView ArticleGoogle Scholar
- Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH: The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 2002, 32: 891-904. 10.1046/j.1365-313X.2002.01474.x.PubMedView ArticleGoogle Scholar
- Taylor NL, Day DA, Millar AH: Targets of stress-induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. J Exp Bot. 2004, 55: 1-10.PubMedView ArticleGoogle Scholar
- Bunik VI, Fernie AR: Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem J. 2009, 422: 405-421. 10.1042/BJ20090722.PubMedView ArticleGoogle Scholar
- Raines CA: The Calvin cycle revisited. Photosynth Res. 2003, 75: 1-10. 10.1023/A:1022421515027.PubMedView ArticleGoogle Scholar
- Henkes S, Sonnewald U, Badur R, Flachmann R, Stitt M: A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell. 2001, 13: 535-551.PubMedPubMed CentralView ArticleGoogle Scholar
- Arora A, Sairam RK, Srivastava GC: Oxidative stress and antioxidative system in plants. Curr Sci. 2002, 82: 1227-1238.Google Scholar
- Couée I, Sulmon C, Gouesbet G, El Amrani A: Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot. 2006, 57: 449-459. 10.1093/jxb/erj027.PubMedView ArticleGoogle Scholar
- Valderrama R, Corpas FJ, Carreras A, Gómez-Rodríguez MV, Chaki M, Pedrajas JR, Fernández-Ocaña A, Del Río LA, Barroso JB: A dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ. 2006, 29: 1449-1459. 10.1111/j.1365-3040.2006.01530.x.PubMedView ArticleGoogle Scholar
- Estevez JM, Cantero A, Reindl A, Reichler S, Leon P: 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem. 2001, 276: 22901-22909. 10.1074/jbc.M100854200.PubMedView ArticleGoogle Scholar
- Lois LM, Rodriguez-Concepcion M, Gallego F, Campos N, Boronat A: Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose5-phosphate synthase. Plant J. 2000, 22: 503-513. 10.1046/j.1365-313x.2000.00764.x.PubMedView ArticleGoogle Scholar
- Paterami I, Kanellis AK: Stress and developmental responses of terpenoid osynthetic genes in Cistus creticus subsp. creticus. Plant Cell Rep. 2010, 29: 629-641. 10.1007/s00299-010-0849-1.View ArticleGoogle Scholar
- Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET: A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol. 2011, 19: 77.View ArticleGoogle Scholar
- Zhu JK: Salt and drought stress signal transduction in plants. Ann Rev Plant Biol. 2002, 53: 247-273. 10.1146/annurev.arplant.53.091401.143329.View ArticleGoogle Scholar
- Cordoba E, Porta H, Arroyo A, San Román C, Medina L, Rodríguez-Concepción M, León P: Functional characterization of the three genes encoding 1-deoxy-D-xylulose 5-phosphate synthase in maize. J Exp Bot. 2011, 62: 2023-2038. 10.1093/jxb/erq393.PubMedView ArticleGoogle Scholar
- Santner A, Estelle M: Recent advances and emerging trends in plant hormone signalling. Nature. 2009, 459: 1071-1078. 10.1038/nature08122.PubMedView ArticleGoogle Scholar
- Peleg Z, Blumwald E: Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol. 2011, 14: 290-295. 10.1016/j.pbi.2011.02.001.PubMedView ArticleGoogle Scholar
- Oh KJ, Park YS, Lee KA, Chung YJ, Cho TJ: Molecular characterization of a thiJ-like gene in Chinese cabbage. J Biochem Mol Biol. 2004, 37: 343-350. 10.5483/BMBRep.2004.37.3.343.PubMedView ArticleGoogle Scholar
- Ahn IP, Kim S, Lee YH: Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol. 2005, 138: 1505-1515. 10.1104/pp.104.058693.PubMedPubMed CentralView ArticleGoogle Scholar
- Bari R, Jones JD: Role of plant hormones in plant defense responses. Plant Mol Biol. 2009, 69: 473-488. 10.1007/s11103-008-9435-0.PubMedView ArticleGoogle Scholar
- Walia H, Wilson C, Wahid A, Condamine P, Cui X, Close TJ: Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genomics. 2006, 6: 143-156. 10.1007/s10142-005-0013-0.PubMedView ArticleGoogle Scholar
- Higo K, Ugawa Y, Iwamoto M, Korenaga T: Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999, 27: 297-300. 10.1093/nar/27.1.297.PubMedPubMed CentralView ArticleGoogle Scholar
- Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y: Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol. 2009, 50: 535-546.View ArticleGoogle Scholar
- Nemhauser JL, Hong F, Chory J: Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006, 126: 467-475. 10.1016/j.cell.2006.05.050.PubMedView ArticleGoogle Scholar
- Arbona V, Argamasilla R, Gómez-Cadenas A: Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol. 2010, 167: 342-1350.View ArticleGoogle Scholar
- Divi UK, Rahman T, Krishna P: Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 2010, 10: 151-10.1186/1471-2229-10-151.PubMedPubMed CentralView ArticleGoogle Scholar
- Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR: Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol. 2010, 61: 651-79. 10.1146/annurev-arplant-042809-112122.PubMedView ArticleGoogle Scholar
- Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K: ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res. 2011, 124: 509-525. 10.1007/s10265-011-0412-3.PubMedView ArticleGoogle Scholar
- Prasad TK, Anderson MD, Stewart CR: Acclimation, Hydrogen Peroxide, and Abscisic Acid Protect Mitochondria against Irreversible Chilling Injury in Maize Seedlings. Plant Physiol. 1994, 105: 619-627.PubMedPubMed CentralGoogle Scholar
- Millar AH, Heazlewood JL: Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis. Plant Physiol. 2003, 131: 443-453. 10.1104/pp.009985.PubMedPubMed CentralView ArticleGoogle Scholar
- Kharenko OA, Boyd J, Nelson KM, Abrams SR, Loewen MC: Identification and characterization of interactions between abscisic acid and mitochondrial adenine nucleotide translocators. Biochem J. 2011, 437: 117-123. 10.1042/BJ20101898.PubMedView ArticleGoogle Scholar
- Bartels D, Sour E: Molecular responses of higher plants to dehydration. Plant responses to abiotic stress. Edited by: Heribert H, Shinozaki K. Springer, Berlin;2004:13-37.Google Scholar
- Shinozaki K, Yamaguchi-Shinozaki K, Seki M: Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol. 2003, 6: 410-417. 10.1016/S1369-5266(03)00092-X.PubMedView ArticleGoogle Scholar
- Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL: A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot. 2005, 56: 2071-2083. 10.1093/jxb/eri206.PubMedView ArticleGoogle Scholar
- Hu ML, Chen YK, Lin YF: The antioxidant and prooxidant activity of some B vitamins and vitamin-like compounds. Chem Bio Interact. 1995, 97: 63-73. 10.1016/0009-2797(95)03608-8.View ArticleGoogle Scholar
- Lukienko PI, Mel'nichenko NG, Zverinskii IV, Zabrodskaya SV: Antioxidant properties of thiamine. Bull Exp Biol Med. 2000, 130: 874-876.PubMedGoogle Scholar
- Bettendorff L, Wins P: Thiamin diphosphate in biological chemistry: new aspects of thiamin metabolism, especially triphosphate derivatives acting other than as cofactors. FEBS J. 2009, 276: 2917-2925. 10.1111/j.1742-4658.2009.07019.x.PubMedView ArticleGoogle Scholar
- Lee BL, Ong HY, Ong CN: Determination of thiamine and its phosphate esters by gradient-elution high-performance liquid chromatography. J Chrom. 1991, 567: 71-80. 10.1016/0378-4347(91)80311-Y.View ArticleGoogle Scholar