Cold acclimation improves photosynthesis by regulating the ascorbate–glutathione cycle in chloroplasts of Kandelia obovata

Weicheng Liu , Chunfang Zheng , Jinong Chen , Jianbiao Qiu , Zhixing Huang , Qi Wang , Yong Ye

Journal of Forestry Research ›› 2019, Vol. 30 ›› Issue (3) : 755 -765.

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Journal of Forestry Research ›› 2019, Vol. 30 ›› Issue (3) : 755 -765. DOI: 10.1007/s11676-018-0791-6
Original Paper

Cold acclimation improves photosynthesis by regulating the ascorbate–glutathione cycle in chloroplasts of Kandelia obovata

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Abstract

As the most northerly mangrove species in China, Kandelia obovata may undergo extreme cold event stress. Enhancing the cold tolerance of this species is crucial to its successful afforestation. This study aimed to determine the resistance of K. obovata seedlings to low temperature stress by cold acclimation and to explain the mechanisms for alleviating cold injury. To understand these mechanisms, seedlings that were acclimatized and not acclimatized were exposed to 5 °C/− 2 °C (day/night) for 48 h. Results showed that low temperature stress reduced leaf photosynthesis of non-acclimatized seedlings by inducing oxidative stress and structural damage to chloroplasts. These phenomena were shown by increasing levels of malondialdehyde (MDA), O2 and H2O2, as well as decreasing enzyme activities in the ascorbate–glutathione (AsA-GSH) cycle. However, cold-acclimatized seedlings had improved photosynthetic rates and efficiency of photosystem II (PSII) under low temperature stress. Compared with non-acclimatized seedlings, leaves of cold-acclimatized seedlings under low temperature stress for 48 h exhibited higher anti-oxidative enzyme activities, lower levels of O2 and H2O2, less damage to chloroplast structure, and removed 33.7% of MDA at low temperature stress for 48 h. The data indicate that cold acclimation enhances photosynthetic capacity by effectively regulating activation in the PSII electron transport and the AsA–GSH cycle to scavenge excess ROS in chloroplasts, while the latter is more important.

Keywords

Ascorbate–glutathione cycle / Cold acclimation / Kandelia obovata / Photosynthesis

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Weicheng Liu, Chunfang Zheng, Jinong Chen, Jianbiao Qiu, Zhixing Huang, Qi Wang, Yong Ye. Cold acclimation improves photosynthesis by regulating the ascorbate–glutathione cycle in chloroplasts of Kandelia obovata. Journal of Forestry Research, 2019, 30(3): 755-765 DOI:10.1007/s11676-018-0791-6

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References

[1]

Alongi DM. Carbon sequestration in mangrove forests. Carbon Manag, 2012, 3: 313-322.

[2]

Ball M, Farquhar G. Photosynthetic and stomatal responses of two mangrove species, Aegiceras corniculatum and Avicennia marina, to long term salinity and humidity conditions. Plant Physiol, 1984, 74: 1-6.

[3]

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem, 1976, 72: 248-254.

[4]

Cakmak I, Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol, 1992, 98: 1222-1227.

[5]

Cheeseman JM, Herendeen LB, Cheeseman AT, Glough BF. Photosynthesis and photoprotection in mangroves under field conditions. Plant Cell Environ, 1997, 20: 579-588.

[6]

Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F. Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep, 2014, 41: 815-822.

[7]

Chen J, Xiao Q, Wang C, Wang W, Wu F, Chen J, He B, Zhu Z, Ru Q, Zhang L, Zheng H. Nitric oxide alleviates oxidative stress caused by salt in leaves of a mangrove species, Aegiceras corniculatum. Aquat Bot, 2014, 117: 41-47.

[8]

Diao M, Ma L, Wang J, Cui J, Fu A, Liu H. Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. J Plant Growth Regul, 2014, 33: 671-682.

[9]

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

[10]

Ellis W, Bowles J, Erickson A, Stafford N, Bell S, Thomas M. Alteration of the chemical composition of mangrove (Laguncularia racemosa) leaf litter fall by freeze damage. Estuar Coast Shelf S, 2006, 68(1–2): 363-371.

[11]

Fei J, Wang Y, Jiang Z, Cheng H, Zhang JD. Identification of cold tolerance genes from leaves of mangrove plant Kandelia obovata by suppression subtractive hybridization. Ecotoxicology, 2015, 24: 1686-1696.

[12]

Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta, 1976, 133: 21-25.

[13]

Garg N, Bhandari P. Interactive effects of silicon and arbuscular mycorrhiza in modulating ascorbate-glutathione cycle and antioxidant scavenging capacity in differentially salt-tolerant Cicer arietinum L. genotypes subjected to long-term salinity. Protoplasma, 2016, 253: 1325-1345.

[14]

Gilman EL, Ellison J, Duke NC, Field C. Threats to mangroves from climate change and adaptation options: a review. Aquat Bot, 2008, 89: 237-250.

[15]

Gupta AS, Webb RP, Holaday AS, Allen RD. Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol, 1993, 103: 1067-1073.

[16]

Holá D, Kutík J, Kočová M, Rothová O. Low-temperature induced changes in the ultrastructure of maize mesophyll chloroplasts strongly depend on the chilling pattern/intensity and considerably differ among inbred and hybrid genotypes. Photosynthetica, 2008, 46: 329-338.

[17]

Hoque MA, Banu MN, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y. Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol, 2007, 164: 1457-1468.

[18]

Jalink H, Schoor R (2015) Role of fluorescence approaches to understand functionanl traits of photosynthesis. In: Phenomics in crop plants: trends, options and limitations. pp 181–194

[19]

Kao WY, Shih CN, Tsai TT. Sensitivity to chilling temperatures and distribution differ in the mangrove species Kandelia candel and Avicennia marina. Tree Physiol, 2004, 24: 859-864.

[20]

Krause G, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Chlorophyll a fluorescence. pp 463–495

[21]

Liu Y, Wang M, Wang W, Fu H, Lu C. Chilling damage to mangrove mollusk species by the 2008 cold event in Southern China. Ecosphere, 2016, 7: e01312.

[22]

Moloi MJ, van der Westhuizen AJ. The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol, 2006, 163: 1118-1125.

[23]

Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Phyiol, 1981, 22: 867-880.

[24]

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

[25]

Peng Y, Wang Y, Fei J, Sun C, Cheng H. Ecophysiological differences between three mangrove seedlings (Kandelia obovata, Aegiceras corniculatum, and Avicennia marina) exposed to chilling stress. Ecotoxicology, 2015, 24: 1-11.

[26]

Perks MP, Osborne B, Mitchell D. Rapid predictions of cold tolerance in Douglas-fir seedlings using chlorophyll fluorescence after freezing. New For, 2004, 28: 49-62.

[27]

Ploschuk EL, Bado LA, Salinas M, Wassner DF, Windauer LB, Insausti P. Photosynthesis and fluorescence responses of Jatropha curcas to chilling and freezing stress during early vegetative stages. Environ Exp Bot, 2014, 102: 18-26.

[28]

Rapacz M. The after-effects of temperature and irradiance during erarly growth of winter oilseed rape (Brassica npus L. var. oleifera, cv. Górczański) seedling on the progress of thier cold acclimation. Acta Physiol Plant, 1998, 20: 73-78.

[29]

Rose RH, Haase D. Chlorophyll fluorescence and variations in tissue cold hardiness in response to freezing stress in Douglas-fir seedlings. New For, 2002, 23: 81-96.

[30]

Shu S, Yuan L, Guo S, Sun J, Yuan Y. Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant physiol Bioch, 2013, 63: 209-216.

[31]

Smith IK. Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol, 1985, 79: 1044-1047.

[32]

Soltész A, Tímár I, Vashegyi I, Tóth B, Kellős T, Szalai G, Vágújfalvi A, Kocsy G, Galiba G. Redox changes during cold acclimation affect freezing tolerance but not the vegetative/reproductive transition of the shoot apex in wheat. Plant Biology, 2011, 13: 757-766.

[33]

Stuart SA, Choat B, Martin KC, Holbrook NM, Ball MC. The role of freezing in setting the latitudinal limits of mangrove forests. New Phytol, 2007, 173: 576-583.

[34]

Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D. Alterations in photosynthesis and antioxidant enzyme activity in winter wheat sujected to post-anthsisi waterlogging. Photosynthetica, 2008, 46: 21-27.

[35]

Thatoi HN, Patra JK, Das SK. Free radical scavenging and antioxidant potential potential of mangrove plants: a review. Acta Physiol Plant, 2014, 36: 561-579.

[36]

Vaculik M, Pavlovic A, Lux A. Silicon alleviates cadmium toxicity by enhanced photosynthetic rate and modified bundle sheath’s cell chloroplasts ultrastructure in maize. Ecotox Environ Saf, 2015, 120: 66-73.

[37]

Vella N, Joss T, Roberts T. Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming. Protoplasma, 2012, 249: 1137-1149.

[38]

Wang W, You S, Wang Y, Huang L, Wang M. Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant Soil, 2010, 342: 105-115.

[39]

Wang X, Cai J, Jiang D, Liu F, Dai T, Cao W. Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J Plant Physiol, 2011, 168: 585-593.

[40]

Yuan L, Shu S, Guo S, Tezuka T. Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplst ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. Photosynth Res, 2012, 112: 205-214.

[41]

Zheng C, Tang J, Chen J, Liu W, Qiu B, Peng X, Ye Y. Mechanisms on inhibition of photosynthesis in Kandelia obovata due to extreme cold events under climate change. Ecol Process, 2016, 5: 20.

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