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Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling

  • Original Papers
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Photosynthetica

Abstract

In order to clarify the relationship between chill-induced disturbance in photosynthetic, respiratory electron transport and the metabolism of reactive oxygen species (ROS), leaf gas exchange, chlorophyll fluorescence quenching, respiration, and activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX) were investigated in chloroplasts and mitochondria of cucumber (Cucumis sativus) leaves subjected to a chill (8 °C) for 4 d. Chilling decreased net photosynthetic rate (P N) and quantum efficiency of photosystem 2 (ΦPS2), but increased the ratio of ΦPS2 to the quantum efficiency of CO2 fixation (ΦCO2) and non-photochemical quenching (NPQ) in cucumber leaves. While chilling inhibited the activity of cytochrome respiration pathway, it induced an increase of alternative respiration pathway activity and the reduction level of Q-pool. Chilling also significantly increased O2 • production rate, H2O2 content, and SOD and APX activities in chloroplasts and mitochondria. There was a more significant increase in SOD and APX activities in chloroplasts than in mitochondria with the increase of membrane-bound Fe-SOD and tAPX in chloroplasts being more significant than other isoenzymes. Taken together, chilling inhibited P N and cytochrome respiratory pathway but enhanced the photosynthetic electron flux to O2 and over-reduction of respiratory electron transport chain, resulting in ROS accumulation in cucumber leaves. Meanwhile, chilling resulted in an enhancement of the protective mechanisms such as thermal dissipation, alternative respiratory pathway, and ROS-scavenging mechanisms (SODs and APXs) in chloroplasts and mitochondria.

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Abbreviations

AOX:

alternative oxidase

APX:

ascorbate peroxidase

AsA:

reduced ascorbate

cAPX:

cytosol APX

Chl:

chlorophyll

Cu/Zn-SOD:

copper-zinc SOD

Fe-SOD:

iron SOD

FM:

fresh mass

mAPX:

microbody APX

Mn-SOD:

manganese SOD

NPQ:

non-photochemical quenching coefficient

O2 •− :

superoxide

Q-pool:

ubiquinone pool

P N :

net photosynthetic rate

PETC:

photosynthetic electron transport chain

PPFD:

photosynthetic photon flux density

PS:

photosystem

RETC:

respiratory electron transport chain

ROS:

reactive oxygen species

sAPX:

stromal APX

SHAM:

salicylhydroxamic acid

SOD:

superoxide dismutase

tAPX:

thylakoid membrane-bound APX

UQ:

the oxidized forms of ubiquinone

UQr:

the reduced forms of ubiquinone

UQr/UQt:

the reduction level of ubiquinone pool

VKCN :

alternative pathway activity

VSHAM :

cytochome pathway activity

Vt :

total respiration

ΦCO2 :

the quantum efficiency of CO2 fixation

ΦPS2 :

quantum efficiency of PS2

References

  • Alscher, R.G., Donahue, J.L., Cramer, C.L.: Reactive oxygen species and antioxidants: relationships in green cells.-Physiol. Plant. 100: 224–233, 1997.

    Article  CAS  Google Scholar 

  • Alscher, R.G., Erturk, N., Heath, L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.-J. exp. Bot. 53: 1331–1341, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Amako, K., Chen, G.-X., Asada, K.: Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isoenzymes of ascorbate peroxidase in plants.-Plant Cell Physiol. 35: 497–504, 1994.

    CAS  Google Scholar 

  • Asada, K.: Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants.-Physiol. Plant. 85: 235–241, 1992.

    Article  CAS  Google Scholar 

  • Asada, K.: The water-water cycle in chloroplasts: Scavenging of active oxygen and dissipation of excess photons.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 601–639, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Asada, K., Takahashi, M.: Production and scavenging of active oxygen in photosynthesis.-In: Kyle, D.J., Osmond, C.B., Arntzen, C.J. (ed.): Photoinhibition. Pp. 227–287. Elsevier, Amsterdam-New York-Oxford 1987.

    Google Scholar 

  • Bartoli, C.G., Gomez, F., Gergoff, G., Guiamét, J.J., Puntarulo, S.: Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions.-J. exp. Bot. 56: 1269–1276, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Bowler, C., Montagu, M.V., Inzé, D.: Superoxide dismutase and stress tolerance.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 83–116, 1992.

    Article  CAS  Google Scholar 

  • Chaumont, M., Morot-Gaudry, J.F., Foyer, C.H.: Effects of photoinhibitory treatment on CO2 assimilation, the quantum yield of CO2 assimilation, D1 protein, ascorbate, glutathione, xanthophylls contents and the electron transport rate in vine leaves.-Plant Cell Environ. 18: 1358–1366, 1995.

    Article  CAS  Google Scholar 

  • Demmig-Adams, B., Adams, W.W., III, Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.-Physiol. Plant. 98: 253–264, 1996.

    Article  CAS  Google Scholar 

  • Fadzillah, N.M., Gill, V., Pinch, R.P., Burdon, R.H.: Chilling, oxidative stress, and antioxidant responses in shoot cultures of rice.-Planta 199: 552–556, 1996.

    Article  CAS  Google Scholar 

  • Foyer, C.H., Vanacker, H., Gomez, L.D., Harbinson, J.: Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review.-Plant Physiol. Biochem. 40: 659–668, 2002.

    Article  CAS  Google Scholar 

  • Fryer, M.J., Andrews, J.R., Oxborough, K., Blowers, D.A., Baker, N.R.: Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature.-Plant Physiol. 116: 571–580, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases occurrence in higher plant.-Plant Physiol. 59: 309–314, 1977.

    Article  PubMed  CAS  Google Scholar 

  • Gómez, J.M., Jiménez, A., Olmos, E., Sevilla, F.: Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts.-J. exp. Bot. 55: 119–130, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson, L., Ball, M.C., Osmond, C.B., Furbank, R.T., Chow, W.S.: Assessment of photoprotection mechanisms of grapevines at low temperature.-Funct. Plant Biol. 30: 631–642, 2003.

    Article  CAS  Google Scholar 

  • Hu, W.H., Shi, K., Song, X.Sh., Xia, X.J., Zhou, Y.H., Yu, J.Q.: Different effects of chilling on respiration in leaves and roots of cucumber (Cucumis sativus).-Plant Physiol. Biochem. 44: 837–843, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Jiménez, A., Hernandez, J.A., del-Rio, L.A., Sevilla, F.: Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves.-Plant Physiol. 114: 275–284, 1997.

    PubMed  Google Scholar 

  • Jiménez, A., Hernández, J.A., Ros, A., Barcelo, L., Sandalio, M., del-Rio, L.A., Sevilla, F.: Mitochondria and peroxisomal ascorbate peroxidase of pea leaves.-Physiol. Plant. 104: 687–692, 1998.

    Article  Google Scholar 

  • Luna, C.M., Pastori, G.M., Driscoll, S., Groten, K., Bernard, S., Foyer, C.H.: Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat.-J. exp. Bot. 56: 417–423, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Luxová, M., Gašpariková, O.: The effect of low temperature on root respiration in maize.-Biológia (Bratislava) 54: 453–458, 1999.

    Google Scholar 

  • Millenaar, F.F., Gonzalez-Meler, M.A., Siedow, J.N., Wagner, A.M., Lambers, H.: 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, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R.: Oxidative stress, antioxidants and stress tolerance.-Trends Plant Sci. 7: 405–410, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., Breusegem, F.V.: Reactive oxygen gene network of plants.-Trends Plant Sci. 9: 490–498, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Mittova, V., Tal, M., Volokita, M., Guy, M.: Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species.-Physiol. Plant. 115: 393–400, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mittova, V., Theodoulou, F.L., Kiddle, G., Volokita, M., Tal, M., Foyer, C.H., Guy, M.: Comparison of mitochondria ascorbate peroxidase in the cultivated tomato, Lycopersicon esculentum, and its wild, salt-tolerant relative, L. pennellii — a role for matrix isoforms in protection against oxidative damage.-Plant Cell Environ. 27: 237–250, 2004.

    Article  CAS  Google Scholar 

  • Mittova, V., Volokita, M., Guy, M., Tal, M.: Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii.-Physiol. Plant. 110: 42–51, 2000.

    Article  CAS  Google Scholar 

  • Møller, I.M.: Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species.-Annu. Rev. Plant Physiol. Plant mol. Biol. 52: 561–591, 2001.

    Article  PubMed  Google Scholar 

  • Neill, S.J., Desikan, R., Clarke, A., Hhrst, R.D., Hancock, J.T.: Hydrogen peroxide and nitric oxide as signaling molecules in plants.-J. exp. Bot. 53: 237–247, 2002.

    Article  Google Scholar 

  • Okamoto, O.K., Robertson, D.L., Fagan, T.F., Hastings, J.W., Colepicolo, P.: Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase.-J. biol. Chem. 276: 19989–19993, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Ort, D.R., Baker, N.R.: A photoprotective role for O2 as an alternative electron sink in photosynthesis?-Curr. Opin. Plant Biol. 5: 193–198, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Purvis, A.C., Shewfelt, R.L.: Does the alternative pathway ameliorate chilling injury in sensitive plant tissues?-Physiol. Plant. 88: 712–718, 1993.

    Article  CAS  Google Scholar 

  • Schöner, S., Krause, G.H.: Protective systems against active oxygen species in spinach: response to cold acclimation in excess light.-Planta 180: 383–389, 1990.

    Article  Google Scholar 

  • Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., Yoshimura, K.: Regulation and function of ascorbate peroxidase isoenzymes.-J. exp. Bot. 53: 1305–1319, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Takeda, T., Yokota, A., Shigeoka, S.: Resistance of photosynthesis to hydrogen peroxide in algae.-Plant Cell Physiol. 36: 1089–1095, 1995.

    CAS  Google Scholar 

  • van Breusegem, F., Slooten, L., Stassart, J.M., Moens, T., Botterman, J., van Montagu, M., Inze, D.; Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize.-Plant Cell Physiol. 40: 515–523, 1999.

    PubMed  Google Scholar 

  • van Camp, W., Capiau, K., van Montagu, M., Inze, D., Slooten, L.: Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts.-Plant Physiol. 112: 1703–1714, 1996.

    Article  PubMed  Google Scholar 

  • Vanlerberghe, G.C., McIntosh, L.: Alternative oxidase: from gene to function.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 703–734, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Wada, K., Tada, T., Nakamura, Y., Ishikawa, T., Yabuta, Y., Yoshimura, K., Shigeoka, S., Nishimura, K.: Crystal structure of chloroplastic ascorbate peroxidase from tobacco plants and structural insights into its instability.-J. Biochem. 134: 239–244, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, A.M., Moore, A.L.: Structure and function of the plant alternative oxidase: its putative role in the oxygen defence mechanism.-Biosci. Rep. 17: 319–333, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, A.M., Wagner, M.J.: Measurements of in vivo ubiquinone reduction levels in plant cells.-Plant Physiol. 108: 277–283, 1995.

    PubMed  CAS  Google Scholar 

  • Yoshida, K., Terashima, I., Noguchi, K.: Distinct role of the cytochrome pathway and alternative oxidase in leaf photosynthesis.-Plant Cell Physiol. 47: 22–31, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura, K., Yabuta, Y., Ishikawa, T., Shigeoka, S.: Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses.-Plant Physiol. 123: 223–233, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Yu, J.Q., Matsui, Y.: Effects of root exudates and allelo-chemical on ion uptake by cucumber seedlings.-J. chem. Ecol. 23: 817–827, 1997.

    Article  CAS  Google Scholar 

  • Zhou, Y.H., Huang, L.F., Du, Y.S., Yu, J.Q.: Greenhouse and field cucumber genotypes use different mechanisms to protect against dark chilling.-Funct. Plant Biol. 31: 1215–1223, 2004a.

    Article  CAS  Google Scholar 

  • Zhou, Y.H., Yu, J.Q., Huang, L.F., Nogués, S.: The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery.-Plant Cell Environ. 27: 1503–1514, 2004b.

    Article  Google Scholar 

  • Zhou, Y.H., Yu, J.Q., Mao, W.H., Huang, L.F., Song, X.S., Nogués, S.: Genotypic variation on Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants.-Plant Cell Physiol. 47: 192–199, 2006.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Horticulture, Huajiachi Campus, Zhejiang University, Kaixuan Road 268, Hangzhou, P.R. China, 310029

    W. H. Hu, X. S. Song, K. Shi, X. J. Xia, Y. H. Zhou & J. Q. Yu

  2. Key Laboratory of Horticultural Plants Growth, Development and Biotechnology, Agricultural Ministry of China, Kaixuan Road 268, Hangzhou, P.R. China, 310029

    J. Q. Yu

  3. Department of Life Science, Jinggangshan University, Ji’an, P.R. China, 343009

    W. H. Hu

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  1. W. H. Hu
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  2. X. S. Song
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  3. K. Shi
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  4. X. J. Xia
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  5. Y. H. Zhou
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  6. J. Q. Yu
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Correspondence to J. Q. Yu.

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Hu, W.H., Song, X.S., Shi, K. et al. Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46, 581–588 (2008). https://doi.org/10.1007/s11099-008-0098-5

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  • DOI: https://doi.org/10.1007/s11099-008-0098-5

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