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.
Similar content being viewed by others
References
Alongi DM (2012) Carbon sequestration in mangrove forests. Carbon Manag 3:313–322
Ball M, Farquhar G (1984) Photosynthetic and stomatal responses of two mangrove species, Aegiceras corniculatum and Avicennia marina, to long term salinity and humidity conditions. Plant Physiol 74:1–6
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Cheeseman JM, Herendeen LB, Cheeseman AT, Glough BF (1997) Photosynthesis and photoprotection in mangroves under field conditions. Plant Cell Environ 20:579–588
Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F (2014a) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep 41:815–822
Chen J, Xiao Q, Wang C, Wang W, Wu F, Chen J, He B, Zhu Z, Ru Q, Zhang L, Zheng H (2014b) Nitric oxide alleviates oxidative stress caused by salt in leaves of a mangrove species, Aegiceras corniculatum. Aquat Bot 117:41–47
Diao M, Ma L, Wang J, Cui J, Fu A, Liu H (2014) Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. J Plant Growth Regul 33:671–682
Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maine leaves. Plant Physiol 114:1031–1037
Ellis W, Bowles J, Erickson A, Stafford N, Bell S, Thomas M (2006) Alteration of the chemical composition of mangrove (Laguncularia racemosa) leaf litter fall by freeze damage. Estuar Coast Shelf S 68(1–2):363–371
Fei J, Wang Y, Jiang Z, Cheng H, Zhang JD (2015) Identification of cold tolerance genes from leaves of mangrove plant Kandelia obovata by suppression subtractive hybridization. Ecotoxicology 24:1686–1696
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25
Garg N, Bhandari P (2016) 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 253:1325–1345
Gilman EL, Ellison J, Duke NC, Field C (2008) Threats to mangroves from climate change and adaptation options: a review. Aquat Bot 89:237–250
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol 103:1067–1073
Holá D, Kutík J, Kočová M, Rothová O (2008) 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 46:329–338
Hoque MA, Banu MN, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007) 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 164:1457–1468
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
Kao WY, Shih CN, Tsai TT (2004) Sensitivity to chilling temperatures and distribution differ in the mangrove species Kandelia candel and Avicennia marina. Tree Physiol 24:859–864
Krause G, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Chlorophyll a fluorescence. pp 463–495
Liu Y, Wang M, Wang W, Fu H, Lu C (2016) Chilling damage to mangrove mollusk species by the 2008 cold event in Southern China. Ecosphere 7:e01312
Moloi MJ, van der Westhuizen AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol 163:1118–1125
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Phyiol 22:867–880
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Peng Y, Wang Y, Fei J, Sun C, Cheng H (2015) Ecophysiological differences between three mangrove seedlings (Kandelia obovata, Aegiceras corniculatum, and Avicennia marina) exposed to chilling stress. Ecotoxicology 24:1–11
Perks MP, Osborne B, Mitchell D (2004) Rapid predictions of cold tolerance in Douglas-fir seedlings using chlorophyll fluorescence after freezing. New For 28:49–62
Ploschuk EL, Bado LA, Salinas M, Wassner DF, Windauer LB, Insausti P (2014) Photosynthesis and fluorescence responses of Jatropha curcas to chilling and freezing stress during early vegetative stages. Environ Exp Bot 102:18–26
Rapacz M (1998) 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 20:73–78
Rose RH, Haase D (2002) Chlorophyll fluorescence and variations in tissue cold hardiness in response to freezing stress in Douglas-fir seedlings. New For 23:81–96
Shu S, Yuan L, Guo S, Sun J, Yuan Y (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant physiol Bioch 63:209–216
Smith IK (1985) Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol 79:1044–1047
Soltész A, Tímár I, Vashegyi I, Tóth B, Kellős T, Szalai G, Vágújfalvi A, Kocsy G, Galiba G (2011) Redox changes during cold acclimation affect freezing tolerance but not the vegetative/reproductive transition of the shoot apex in wheat. Plant Biology 13:757–766
Stuart SA, Choat B, Martin KC, Holbrook NM, Ball MC (2007) The role of freezing in setting the latitudinal limits of mangrove forests. New Phytol 173:576–583
Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat sujected to post-anthsisi waterlogging. Photosynthetica 46:21–27
Thatoi HN, Patra JK, Das SK (2014) Free radical scavenging and antioxidant potential potential of mangrove plants: a review. Acta Physiol Plant 36:561–579
Vaculik M, Pavlovic A, Lux A (2015) Silicon alleviates cadmium toxicity by enhanced photosynthetic rate and modified bundle sheath’s cell chloroplasts ultrastructure in maize. Ecotox Environ Saf 120:66–73
Vella N, Joss T, Roberts T (2012) Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming. Protoplasma 249:1137–1149
Wang W, You S, Wang Y, Huang L, Wang M (2010) Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant Soil 342:105–115
Wang X, Cai J, Jiang D, Liu F, Dai T, Cao W (2011) Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J Plant Physiol 168:585–593
Yuan L, Shu S, Guo S, Tezuka T (2012) Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplst ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. Photosynth Res 112:205–214
Zheng C, Tang J, Chen J, Liu W, Qiu B, Peng X, Ye Y (2016) Mechanisms on inhibition of photosynthesis in Kandelia obovata due to extreme cold events under climate change. Ecol Process 5:20
Author information
Authors and Affiliations
Corresponding authors
Additional information
Project funding: This research was supported by Zhejiang Provincial Natural Science Foundation of China (Grant Nos. LY18C030001 and LQ13C030002), National Natural Science Foundation of China (Grant No. 41776097), Special Funding for Research of National Oceanic Public Service Industry of China (Grant No. 201505028), National Science and Technology Basic Resources Survey Special of China (Grant No. 2017FY100700), Zhejiang Province Science and Technology Plan Project of China (Grant Nos. 2013C25096 and 2014F50003), Zhejiang Province Foundation of the Nonprofit Technology Research Projects of China (Grant No. 2015C33227) and Wenzhou Municipal Science and Technology Plan Project of China (Grant Nos. N20140046, N20170008 and S20160004).
The online version is available at http://www.springerlink.com
Corresponding editor: Hu Yanbo.
Rights and permissions
About this article
Cite this article
Liu, W., Zheng, C., Chen, J. et al. Cold acclimation improves photosynthesis by regulating the ascorbate–glutathione cycle in chloroplasts of Kandelia obovata. J. For. Res. 30, 755–765 (2019). https://doi.org/10.1007/s11676-018-0791-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11676-018-0791-6