Skip to main content
Log in

Mitochondrial uncoupling protein silence is compromised in photosynthesis and redox poise

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Mitochondrial uncoupling proteins play important roles in generation of metabolic thermogenesis, response to stress situations, and regulation of energy metabolism. We demonstrated here that the absence of LeUCP in tomato inhibited photosynthesis using virus-induced gene-silencing approach. A significant decrease in the rate of CO2 assimilation in LeUCP-silencing plants was observed over a range of different light intensities. Absence of LeUCP resulted in lower net photosynthetic rate, light-saturated rate of the CO2 assimilation (A sat), maximum carboxylation rates (V cmax) and maximum RuBP regeneration rate (J max). Activities of ribulose-1,5-bisphosphate carboxylase/oxygenase Rubisco and stromal fructose-1,6-bisphosphatase and genes expression levels encoded Calvin cycle enzymes of LeUCP gene-silencing plants were inhibited. However, silencing of LeUCP gene had no effect on F v/F m, but decreased photochemical quenching and electron transport rate. Meanwhile, non-photochemical quenching and Je (PSII), the distribution of Je (PCR) and Je (PCO), the content of AsA, NAD, and the ratios of NAD+/NADH, AsA/DHA were significantly reduced with increased reactive oxygen species while GSH and GSSG were unaltered. Taken together, these results strongly suggest that LeUCP gene in tomato leaves is crucial in maintaining the redox poise of the mitochondrial electron transport chain to facilitate photosynthetic metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  PubMed  CAS  Google Scholar 

  • Begcy K, Mariano ED, Mattiello L, Nunes AV, Mazzafera P, Maia IG, Menossi M (2011) An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants. PLoS ONE 6:e23776

    Article  PubMed  CAS  Google Scholar 

  • Bestwick CS, Brown IR, Bennett MHR, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9:209–221

    PubMed  CAS  Google Scholar 

  • Borecky J, Vercesi AE (2005) Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Bioscience Rep 25:271–286

    Article  CAS  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    Article  PubMed  CAS  Google Scholar 

  • Chen JC, Jiang CZ, Gookin TE, Hunter DA, Clark DG, Reid MS (2004) Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol Biol 55:521–530

    Article  PubMed  CAS  Google Scholar 

  • Cui JX, Zhou YH, Ding JG, Xia XJ, Shi K, Chen SC, Asami T, Chen ZX, Yu JQ (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant, Cell Environ 34:347–358

    Article  CAS  Google Scholar 

  • Dai AH, Nie YX, Yu B, Li Q, Lu LY, Bai JG (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10

    Article  CAS  Google Scholar 

  • Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    Article  PubMed  CAS  Google Scholar 

  • Dietz K-J, Pfannschmidt T (2011) Novel Regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485

    Article  PubMed  CAS  Google Scholar 

  • Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037

    PubMed  CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium-chloride—simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  PubMed  CAS  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Filella I, Llusia J, Pinol J, Penuelas J (1998) Leaf gas exchange and fluorescence of Phillyrea latifolia, Pistacia lentiscus and Quercus ilex saplings in severe drought and high temperature conditions. Environ Exp Bot 39:213–220

    Article  Google Scholar 

  • Foyer CH, Theodoulou FL, Delrot S (2001) The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci 6:486–492

    Article  PubMed  CAS  Google Scholar 

  • Harbinson J, Genty B, Foyer CH (1990) Relationship between photosynthetic electron-transport and stromal enzyme-activity in pea leaves—toward an understanding of the nature of photosynthetic control. Plant Physiol 94:545–553

    Article  PubMed  CAS  Google Scholar 

  • Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 27:1853–1856

    Article  Google Scholar 

  • Jarmuszkiewicz W, Woyda-Ploszczyca A, Antos-Krzeminska N, Sluse FE (2010) Mitochondrial uncoupling proteins in unicellular eukaryotes. BBA Bioenerg 1797:792–799

    Article  CAS  Google Scholar 

  • Jezek P, Hanus J, Semrad C, Garlid KD (1996) Photoactivated azido fatty acid irreversibly inhibits anion and proton transport through the mitochondrial uncoupling protein. J Biol Chem 271:6199–6205

    Article  PubMed  CAS  Google Scholar 

  • Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Bio 6:248–261

    Article  CAS  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic-acid in spinach (Spinacia oleracea) chloroplasts—the effect of hydrogen-peroxide and of Paraquat. Biochem J 210:899–903

    PubMed  CAS  Google Scholar 

  • Lilley RM, Walker DA (1974) An improved spectrophotometric assay for ribulose-bisphosphate carboxylase. Biochim Biophys Acta 358:226–229

    Article  PubMed  CAS  Google Scholar 

  • Liu YL, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Maia IG, Benedetti CE, Leite A, Turcinelli SR, Vercesi AE, Arruda P (1998) AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein. FEBS Lett 429:403–406

    Article  PubMed  CAS  Google Scholar 

  • Maxwell DP, Nickels R, McIntosh L (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J 29:269–279

    Article  PubMed  CAS  Google Scholar 

  • Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367

    Article  PubMed  CAS  Google Scholar 

  • Miyake C, Yokota A (2000) Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis. Plant Cell Physiol 41:335–343

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Nogueira FTS, Sassaki FT, Maia IG (2011) Arabidopsis thaliana Uncoupling Proteins (AtUCPs): insights into gene expression during development and stress response and epigenetic regulation. J Bioenerg Biomembr 43:71–79

    Article  PubMed  CAS  Google Scholar 

  • Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052

    Article  PubMed  CAS  Google Scholar 

  • Ozawa K, Murayama S, Kobayashi-Uehara A, Handa H (2006) Overexpression of wheat mitochondrial uncoupling protein in rice plants confers tolerances to oxidative stresses promoted by exogenous hydrogen peroxide and low temperature. Mol Breed 18:51–56

    Google Scholar 

  • Perez-Lopez U, Robredo A, Lacuesta M, Sgherri C, Mena-Petite A, Navari-Izzo F, Munoz-Rueda A (2010) Lipoic acid and redox status in barley plants subjected to salinity and elevated CO2. Physiol Plantarum 139:256–268

    CAS  Google Scholar 

  • Pfannschmidt T, Braeutigam K, Wagner R, Dietzel L, Schroeter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103:599–607

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Fletcher JE, Barnes J, Foyer CH (2003) The function of ascorbate oxidase (AO) in tobacco (Nicotiana tabacum L.). Plant Physiol 132:1631–1641

    Article  PubMed  CAS  Google Scholar 

  • Popov VN, Eprintsev AT, Maltseva EV (2011) Activation of genes encoding mitochondrial proteins involved in alternative and uncoupled respiration of tomato plants treated with low temperature and reactive oxygen species. Russ J Plant Physiol 58:914–920

    Article  CAS  Google Scholar 

  • Rao MV, Ormrod DP (1995) Impact of UVB and O3 on the oxygen-free radical scavenging system in Arabidopsis thaliana genotypes differing in flavonoid biosynthesis. Photochem Phorobiol 62:719–726

    Article  CAS  Google Scholar 

  • Ryrie IJ, Scott KJ (1968) Metabolic regulation in diseased leaves II. changes in nicotinamide nucleotide coenzymes in barley leaves infected with powdery mildew. Plant Physiol 43:687–692

    Article  PubMed  CAS  Google Scholar 

  • Scheibe R, Fickenscher K, Ashton AR (1986) Studies on the mechanisms of the reductive activation of NADP-malate dehydrogenase by thioredoxin m and low molecular weight thiols. Biochim Biophys Acta 870:191–197

    Article  CAS  Google Scholar 

  • Schonhof I, Kläring HP, Krumbein A, Clau beta ben W, Schreiner M (2007) Effect of temperature increase under low radiation conditions on phytochemicals and ascorbic acid in greenhouse grown broccoli. Agr Ecosyst Environ 119:103–111

    Article  CAS  Google Scholar 

  • Sharkey TD, Savitch LV, Butz ND (1991) Photometric method for routine determination of kcat and carbamylation of Rubisco. Photosynth Res 28:41–48

    Article  CAS  Google Scholar 

  • Shi K, Dine XT, Dong DK, Zhou YH, Yu JQ (2008) Putrescine enhancement of tolerance to root-zone hypoxia in Cucumis sativus: a role for increased nitrate reduction. Funct Plant Biol 35:337–345

    Article  CAS  Google Scholar 

  • Sluse F, Jarmuszkiewicz W, Navet R, Douete P, Mathy G, Sluse-Goffart CM (2006) Mitochondrial UCPs: new insights into regulation and impact. BBA Bioenerg 5–6:480–485

    Article  Google Scholar 

  • Smith AMO, Ratcliffe RG, Sweetlove LJ (2004) Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 279:51944–51952

    Article  PubMed  CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plantarum 142(1):56–64

    Article  CAS  Google Scholar 

  • Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 103:19587–19592

    Article  PubMed  CAS  Google Scholar 

  • Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446

    Article  PubMed  CAS  Google Scholar 

  • Talbot DA, Brand MD (2005) Uncoupling protein 3 protects aconitase against inactivation in isolated skeletal muscle mitochondria. Biochim Biophys Acta 1709:150–156

    PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang ZG, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Trono D, Flagella Z, Laus MN, Di Fonzo N, Pastore D (2004) The uncoupling protein and the potassium channel are activated by hyperosmotic stress in mitochondria from durum wheat seedlings. Plant Cell Environ 27:437–448

    Article  CAS  Google Scholar 

  • Vercesi AE, Borecky J, Godoy Maia ID, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Ann Rev Plant Biol 57:383–404

    Article  CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, VanMontagu M, Inze D, VanCamp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  PubMed  CAS  Google Scholar 

  • Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920

    Article  CAS  Google Scholar 

  • Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen ZX, Yu JQ (2009a) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196

    Article  PubMed  CAS  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen ZX, Yu JQ (2009b) Reactive oxygen species are involved in Brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  PubMed  CAS  Google Scholar 

  • Yosef I, Irihimovitch V, Knopf JA, Cohen I, Orr-Dahan I, Nahum E, Keasar C, Shapira M (2004) RNA binding activity of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J Biol Chem 279:10148–10156

    Article  PubMed  CAS  Google Scholar 

  • Zhou YH, Yu JQ, Mao WH, Huang LF, Song XS, Nogues S (2006) Genotypic variation of rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants. Plant Cell Physiol 47:192–199

    Article  PubMed  CAS  Google Scholar 

  • Zhou YH, Lam HM, Zhang JH (2007) Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot 58:1207–1217

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Lu JF, Wang J, Chen F, Leng FF, Li HY (2011) Regulation of thermogenesis in plants: the interaction of alternative oxidase and plant uncoupling mitochondrial protein. J Integr Plant Biol 53:7–13

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (31071790, 31101536), Science Development Plan Project of Shandong Province (2012GNC011111), Outstanding Young Teacher Project in Henan Province (2011GGJS-075), National Basic Research Program of China (2009CB119000), National Natural Science Foundation of China (31071790; 31101536) and the National Key Technology R&D Program of China (2011BAD12B03).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shuangchen Chen.

Additional information

Communicated by Z. Gombos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, S., Jin, W., Liu, Ar. et al. Mitochondrial uncoupling protein silence is compromised in photosynthesis and redox poise. Acta Physiol Plant 35, 2547–2558 (2013). https://doi.org/10.1007/s11738-013-1290-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-013-1290-1

Keywords

Navigation