Inhibition of the alternative respiratory pathway at high temperatures leads to higher reactive oxygen species production and downregulation of the antioxidant defense system in squash leaves

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• 作者：Neelam Ara ; Naveedullah ; Changqing Ding ; Jinghua Yang…
• 关键词：Alternative oxidase ; Thermotolerance ; Heat stress ; Pumpkin ; Antioxidant enzymes
• 刊名：Plant Growth Regulation
• 出版年：2016
• 出版时间：May 2016
• 年：2016
• 卷：79
• 期：1
• 页码：127-134
• 全文大小：788 KB
• 参考文献：Almeselmani M, Deshmukh P, Sairam R, Kushwaha S, Singh T (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171(3):382–388CrossRef PubMed
  Amirsadeghi S, Christine AR, 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(11):1509–1519CrossRef PubMed
  Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRef PubMed
  Ara N, Yang J, Hua Z, Zhang M (2013) Determination of heat tolerance of interspecific (Cucurbita maxima × Cucurbita moschata) inbred line of squash ‘Maxchata’ and its parents through photosynthetic response. J Agric Sci 19:188–197
  Camejo D, Jiménez A, Alarcón JJ, Torres W, Gómez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct Plant Biol 33:177–187CrossRef
  Casolo V, Braidot E, Chiandussi E, Macrì F, Vianello A (2000) The role of mild uncoupling and non-coupled respiration in the regulation of hydrogen peroxide generation by plant mitochondria. FEBS Lett 474:53–57CrossRef PubMed
  Czarna M, Jarmuszkiewicz W (2005) Activation of alternative oxidase and uncoupling protein lowers hydrogen peroxide formation in amoeba Acanthamoeba castellanii mitochondria. FEBS Lett 579:3136–3140CrossRef PubMed
  Dmitry BZ, Boris FK, Alevtina EK, Michail YV, Ljubava DZ (1997) Mitochondria revisited. Alternative functions of mitochondria. Biosci Rep 17(6):507–520CrossRef
  Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15(5):1212–1226CrossRef PubMed PubMedCentral
  Ederli L, Morettini R, Borgogni A, Wasternack C, Miersch O, Reale L, Ferranti F, Tosti N, Pasqualini S (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142:595–608CrossRef PubMed PubMedCentral
  Fiorani F, Umbach LA, Siedow NJ (2005) The AOX of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 139:1795–1805CrossRef PubMed PubMedCentral
  Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRef PubMed
  Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of AOX1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610CrossRef PubMed PubMedCentral
  Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46(4):581–588CrossRef
  Hu W, Xiao Y, Zeng J, Hu X (2010) Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. Biol Plant 54:761–765CrossRef
  Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42(11):1265–1273CrossRef PubMed
  Kiraly L, Hafez YM, Fodor J, Kiraly Z (2008) Suppression of Tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J Gen Virol 89:799–808CrossRef PubMed
  Lambers H (1997) Oxidation of mitochondrial NADH and the synthesis of ATP. In: Dennis DT, Layzell DB, Lefebvre DD, Turpin DH (eds) Plant metabolism. Longman, Singapore, pp 200–219
  Li Y, Zhu L, Xu B, Yang J, Zhang M (2012) Identification of down-regulated genes modulated by an alternative oxidase pathway under cold stress conditions in watermelon. Plant Mol Biol Rep 30:214–224CrossRef
  Lin TY, Markhart HA (1990) Temperature effects on mitochondrial respiration in Phaseolus acutifolius A. Gray and Phaseolus vulgaris L. Plant Physiol 94:54–58CrossRef PubMed PubMedCentral
  Maxwell DP, Wang Y, McIntosh L (1999) The AOX lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci 96:8271–8276CrossRef PubMed PubMedCentral
  Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRef PubMed
  Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481CrossRef PubMed
  Pasqualini S, Paolocci F, Borgogni A, Morettini R, Ederli L (2007) The overexpression of an alternative oxidase gene triggers ozone sensitivity in tobacco plants. Plant Cell Environ 30:1545–1556CrossRef PubMed
  Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29(9):e45–e45CrossRef PubMed PubMedCentral
  Plaxton WC, Podesta FE (2006) The functional organization and control of plant respiration. Critical Rev Plant Sci 25:159–198CrossRef
  Polidoros AN, Mylonab PV, Arnholdt-Schmittc B (2009) AOX gene structure, transcript variation and expression in plants. Physiol Plant 137:342–353CrossRef PubMed
  Popov VN, Simonian RA, Skulachev VP, Starkov AA (1997) Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Lett 415:87–90CrossRef PubMed
  Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol Plant 100:165–170CrossRef
  Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 55:23–39CrossRef PubMed
  Rhoads DM, Vanlerberghe GC (2004) Mitochondria–nucleus interactions: evidence for mitochondrial retrograde communication in plant cells. In: Day DA, Millar AH, Whelan J (eds) Advances in photosynthesis and respiration, vol 17. Kluwer Academic Publishers, Dordrecht, pp 83–106
  Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366CrossRef PubMed PubMedCentral
  Sambrook J, Fritsch EF, Maniati T (1989) Molecular cloning, vol 2. Cold Spring Harbor Laboratory Press, New York
  Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered AOX levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139(4):1806–1820CrossRef PubMed PubMedCentral
  Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants, protective role of exogenous polyamines. Plant Sci 151(1):59–66CrossRef
  Wang HH, Liang XL, Huang JJ, Zhang DK, Lu HX, Liu ZJ, Bi YR (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis Calluses. Plant Cell Physiol 51:1754–1765CrossRef PubMed
  Watanabe CK, Hachiya T, Terashima I, Noguchi K (2008) The lack of AOX at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of anti-oxidant defense systems in Arabidopsis thaliana leaves. Plant Cell Environ 31:1190–1202CrossRef PubMed
  Woodson JD, Chory J (2008) Coordination between organellar and nuclear genomes. Nat Rev Genet 9:383–395CrossRef PubMed
  Yip JYH, Vanlerberghe GC (2001) Mitochondrial AOX acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol Plant 112:327–333CrossRef PubMed
  Zhang L, Oh Y, Li H, Baldwin IT, Galis I (2012) Alternative oxidase in resistance to biotic stresses: Nicotiana attenuata AOX contributes to resistance to a pathogen and a piercing-sucking insect but not Manduca sexta larvae. Plant Physiol 60:1453–1467
  Zhu L, Li Y, Ara N, Yang J, Zhang M (2012) Role of a newly cloned alternative oxidase gene (BjAOX1a) in turnip mosaic virus (TuMV) resistance in mustard. Plant Mol Biol Rep 30(2):309–318CrossRef
  
• 作者单位：Neelam Ara (1) (2) (3)
  Naveedullah (4) (5)
  Changqing Ding (1) (2)
  Jinghua Yang (1) (2)
  Zhongyuan Hu (1) (2)
  Mingfang Zhang (1) (2)
  
  1. Laboratory of Genetic Resources and Functional Improvement for Horticultural Plants, Department of Horticulture, Zhejiang University, Hangzhou, 310058, Zhejiang Province, People’s Republic of China
  2. Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Hangzhou, 310058, People’s Republic of China
  3. Department of Horticulture, The University of Agriculture, Peshawar, Pakistan
  4. Department of Environmental Engineering, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, People’s Republic of China
  5. Department of Water Management, The University of Agriculture, Peshawar, Pakistan
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Physiology
  
• 出版者：Springer Netherlands
• ISSN：1573-5087

文摘

In this work, the role of the alternative respiratory pathway in the heat tolerance of squashes was determined. Heat-tolerant C. moschata, heat-susceptible C. maxima and intermediate heat-tolerant ‘Maxchata’ plants were sprayed with an inhibitor of the alternative respiratory pathway, 2 mM salicylhydroxamic acid (SHAM), or water and were subjected to three different temperatures, i.e., 30 °C (control), 37 °C daytime temperature (moderate heat stress) or 42 °C daytime temperature (severe heat stress), for 7 days. The results indicated that total, cytochrome and alternative respirations were high in C. moschata and ‘Maxchata’ at both 37 and 42 °C, but decreased in C. maxima at 42 °C. Moreover, the increase in reactive oxygen species production upon heat exposure was also more apparent in SHAM-treated squashes compared with water-treated ones. The transcript levels of APX1, APX2,CAT1, CAT2, CAT3, Cu/ZnSOD, FeSOD and MnSOD were determined in both the SHAM- and water-treated squash leaves that were exposed to heat stress. It was observed that CAT1 and FeSOD were downregulated in SHAM-treated C. moschata plants under heat stress conditions. In addition, the expressions of CAT2 and MnSOD were lower in SHAM-treated C. moschata and ‘Maxchata’ plants. These results indicate some type of interrelationship between AOX and antioxidant systems. However, the complexity of the regulatory mechanisms and their contribution to the stress tolerance of squashes requires further research.