Silencing of mitochondrial uncoupling protein gene aggravates chilling stress by altering mitochondrial respiration and electron transport in tomato

• Autorzy: Liu A. , Chen S. , Wang M. , Wang Z. , Zheng C. , Zhao P. , Guo D. , Ahammed G.J.
• Języki publikacji: EN

Abstrakty

EN

Mitochondrial uncoupling proteins (UCPs) play crucial role in the regulation of metabolic thermogenesis, photosynthesis, redox poise, and response to stress situations. However, the involvements UCPs and its regulatory mechanisms in plant mitochondrial respiration and electron transport have not yet been fully substantiated. In this article, we show that UCP is essential for effective respiratory balance and mitochondrial electron transport poise under chilling stress in tomato. Compared with pTRV (non-silenced) plants, suppression of LeUCP the expression by virus-induced gene silencing significantly decreased the total, SHAM-resistant, and CN-resistant respiratory rates, but increased cytosolic glycolysis pathway- related gene expression and enzymes’ activities under chilling stress. The transcripts’ abundances of UCRH, COX1, COX2, AOX1a, AOX2, and NDC1 genes involved in main and bypass miETC components were decreased, while those of NDUO and SDH4 were slightly increased in the leaves of LeUCP-silenced plants. In addition, silencing of LeUCP aggravated H2O2 and O2- accumulation levels in leaves under chilling stress. Our results provide strong evidence that LeUCP is critical for respiratory homeostasis and mitochondrial electron transport signaling under chilling stress in tomato.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 11
• Opis fizyczny: Article: 223 [9 p.], fig.,ref.

Twórcy

autor

Liu A.

• College of Forestry, Henan University of Science and Technology, No. 70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China

autor

Chen S.

• College of Forestry, Henan University of Science and Technology, No. 70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China
• Department of Plant Science, Agricultural and Animal Husbandry College of Tibet University, Xueyuan Road, Linzhi, 860000, People’s Republic of China

autor

Wang M.

• College of Forestry, Henan University of Science and Technology, No. 70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China

autor

Wang Z.

• Department of Plant Science, Agricultural and Animal Husbandry College of Tibet University, Xueyuan Road, Linzhi, 860000, People’s Republic of China

autor

Zheng C.

• College of Forestry, Henan University of Science and Technology, No. 70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China

autor

Zhao P.

• College of Horticulture, South China Agricultural University, Guangzhou, 510642, Guangdong, People’s Republic of China

autor

Guo D.

• College of Forestry, Henan University of Science and Technology, No. 70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China

autor

Ahammed G.J.

• Department of Horticulture, Zijingang Campus, Zhejiang University, Yuhangtang Road 866, Hangzhou, 310058, People’s Republic of China

Bibliografia

• Amirsadeghi S, Robson CA, McDonald AE, Vanlerberghe GC (2006) Changes in plant mitochondrial electron transport alter cellular levels of reactive oxygen species and susceptibility to cell death signaling molecules. Plant Cell Physiol 47:1509–1519
• Atkin OK, Scheurwater I, Pons TL (2006) High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Glob Change Biol 12:500–515
• Barreto P, Neschich IAP, Okura V, Maia IG, Arruda P (2014) Overexpression of UCP1 in tobacco induces mitochondrial biogenesis through retrograde signaling and amplifies a broad stress response. BMC Plant Biol 14:1–31
• 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
• Borecky J, Vercesi AE (2005) Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Biosci Rep 25:271–286
• Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60:1823–1837
• Chen SC, Jin WJ, Liu AR, Liu ZM, Liu DL, Xia XJ, Lin XM (2013a) Mitochondrial uncoupling protein silence is compromised in photosynthesis and redox poise. Acta Physiol Plant 35:2547–2558
• Chen SC, Liu AR, Zhang SJ, Li C, Chang R, Liu DL, Ahammed GJ, Lin XM (2013b) Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress and Botrytis cinerea infection in tomato. Plant Physiol Biochem 73:245–253
• Chen SC, Liu AR, Ji DG, Lin XM, Liu ZM, Xia XJ, Liu DL, Ahammed GJ (2014) Silencing of tomato mitochondrial uncoupling protein disrupts redox poise and antioxidant enzymes activities balance under oxidative stress. J Plant Biol 57:9–19
• Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of nonphosphorylating bypasses. BBA-Bioenergetics 1757:730–741
• Considine MJ, Daley DO, Whelan J (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiol 126:1619–1629
• Daley DO, Considine MJ, Howell KA, Millar AH, Day DA, Whelan J (2003) Respiratory gene expression in soybean cotyledons during post-germinative development. Plant Mol Biol 51:745–755
• del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335
• Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037
• Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415:96–99
• Ekengren SK, Liu Y, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36:905–917
• Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium-chloride-simple assay for superoxide dismutase. Anal Biochem 70:616–620
• Escobar MA, Geisler DA, Rasmusson AG (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J 45:775–788
• Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254–261
• Figueira TRS, Arruda P (2011) Differential expression of uncoupling mitochondrial protein and alternative oxidase in the plant response to stress. J Bioenerg Biomembr 43:67–70
• Florez-Sarasa I, Flexas J, Rasmusson AG, Umbach AL, Siedow JN, Ribas-Carbo M (2011) In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant, Cell Environ 34:1373–1383
• Grabelnych OI, Borovik OA, Tauson EL, Pobezhimova TP, Katyshev AI, Pavlovskaya NS, Koroleva NA, Lyubushkina IV, Bashmakov VYu, Popov VN, Borovskii GB, Voinikov VK (2014) Mitochondrial energy_dissipating systems (alternative oxidase, uncoupling proteins, and external NADH dehydrogenase) are involved in development of frost_resistance of winter wheat seedlings. Biochemistry (Moscow) 79:506–519
• Jarmuszkiewicz W, Woyda-Ploszczyca A, Antos-Krzeminska N, Sluse FE (2010) Mitochondrial uncoupling proteins in unicellular eukaryotes. BBA-Bioenergetics 1797:792–799
• Jezek P, Borecký J, Zácková M, Costa AD, Arruda P (2001) Possible basic and specific functions of plant uncoupling proteins (pUCP). Biosci Rep 21:237–245
• Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systeminmediated defense response against herbivorous insects. Proc Natl Acad Sci USA 104:12205–12210
• Kowaltowski AJ, Castilho RF, Vercesi AE (1996) Opening of the mitochondrial permeability transition pore by uncoupling or inorganic phosphate in the presence of Ca2+ is dependent on mitochondrial-generated reactive oxygen species. FEBS Lett 378:150–152
• Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Bio 6:248–261
• Li X, Zhang GQ, Sun B, Zhang S, Zhang YQ, Liao YWK, Zhou YH, Xia XJ, Shi K, Yu JQ (2013) Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere. Sci Rep 3:3433
• Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25:402–408
• Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104
• Millenaar FF, Gonzalez-Meler MA, Siedow JN, Wagner AM, Lambers H (2002) Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots. J Exp Bot 53:1081–1088
• Mutuku JM, Nose A (2012) Changes in the contents of metabolites and enzyme activities in rice plants responding to Rhizoctonia solani Kuhn infection: activation of glycolysis and connection to phenylpropanoid pathway. Plant Cell Physiol 53:1017–1032
• Navrot N, Roubier N, Gelbaye E, Jacquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195
• 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
• Panda SK, Sahoo L, Katsuhara M, Matsumoto H (2013) Overexpression of alternative oxidase gene confers aluminum tolerance by altering the respiratory capacity and the response to oxidative stress in tobacco cells. Mol Biotechnol 54:551–563
• Plaxton WC (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198
• 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
• Schwarzländer M, König AC, Sweetlove LJ, Finkemeier I (2012) The impact of impaired mitochondrial function on retrograde signalling: a meta-analysis of transcriptomic responses. J Exp Bot 63:1735–1750
• Shi K, Fu LJ, Zhang S, Li X, Liao YWK, Xia XJ, Zhou YH, Wang RQ, Chen ZX, Yu JQ (2013) Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants. Planta 237:589–601
• Smith AMO, Ratcliffe RG, Sweetlove Lee J (2004) Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 279:51944–51952
• 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
• Vanlerberghe GC, McIntosh L (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol 100:115–119
• Vercesi AE, Borecky J, Godoy Maia ID, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 57:383–404
• Vianello A, Macri F, Braidot E, Mokhova EN (1995) Effect of 6-ketocholestanol on FCCP- and DNP-induced uncoupling in plant mitochondria. FEBS Lett 365:7–9
• Watanabe CK, Hachiya T, Terashima I, Noguchi K (2008) The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an upregulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant, Cell Environ 31:1190–1202
• 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
• Zeng Y, Wu Y, Avigne WT, Koch KE (1998) Differential regulation of sugar-sensitive sucrose syntheses by hypoxia and anoxia indicate complementary transcriptional and post-transcriptional responses. Plant Physiol 116:1573–1583
• Zhao ZX, Assmann SMJ (2011) The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J Exp Bot 62:5179–5189
• 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

Identyfikatory

DOI

10.1007/s11738-015-1974-9