Response of leaf photosynthetic characteristics of Syringa oblata and Syringa reticulata var. mandshurica to chilling stress

Abstract

Syringa species not only have good ornamental properties but also play an important role in the landscaping and environmental purification of cities. To investigate the chilling stress resistance of Syringa oblata Lindl. and Syringa reticulata var. mandshurica and provide theoretical grounds for the practical cultivation of Syringa species, in vitro leaves were used to study photosynthetic gas exchange parameters and chlorophyll fluorescence parameters. After nine hours of chilling, decreasing rates of net photosynthesis, stomatal conductance, and transpiration in S. reticulata var. mandshurica leaves were significantly greater than that of the S. oblata, while intercellular CO₂ concentrations in S. oblata leaves were higher than those in S. reticulata var. mandshurica. The quantum yield of PSII reaction center (Ф _PSII) declined in S. reticulata and light capture efficiency (F _v′/F _m′) was stable. However, reduction percentages of F _v′/F _m′, Ф _PSII, and F _v/F _m in S. oblata were significant higher than those of S. reticulata var. mandshurica. After nine hours of chilling, the relative variable fluorescence of V _J and V _I of S. oblata increased and the increasing rate of V _J was greater than V _I. In contrast, the change of V _J and V _I in S. reticulata var. mandshurica leaves was relatively small. This suggests that chilling primarily damaged the electron transport process of Q_A to Q_B at the receptor site of the PSII reaction center. Photosynthetic capacity of S. oblata was more sensitive to chilling stress compared to S. reticulate var. mandshurica, which the limitations were mainly due to non-stomatal factors such as the decrease in electron transport efficiency, activity in the PSII reaction center, and the destruction of the photodamage defense system.

Keywords

Chilling stress / Chlorophyll fluorescence characteristics / Photosynthetic capacity / Syringa oblate / Syringa reticulata var. mandshurica

References

[1] Ahmed S, Nawata E, Hosokawa M, Domae Y, Sakuratani T. Alterations in photosynthesis and some antioxidant enzymatic activities of mungbean subjected to water logging. Plant Sci, 2002, 163(1): 117-123.

[2] Allahverdiyeva Y, Suorsa M, Rossi F, Pavesi A, Kater MM, Antonacci A, Tadini L, Pribil M, Schneider G, Wanner D, Leister EM, Aro R, Barbato R, Pesaresi P. Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII supercomplex organization and short-term adaptive mechanisms. Plant J, 2013, 75(4): 671-684.

[3] Allen DJ, Ort DR. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci, 2001, 6: 36-41.

[4] Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol, 2006, 141(2): 391-396.

[5] Ashraf M, Arfan M. Gas exchange characteristics and water relations in two cultivars of Hibiscus esculentus under waterlogging. Biol Plant, 2005, 49(3): 459-462.

[6] Ashraf M, Harris PJC. Photosynthesis under stressful environments: an overview. Photosynthetica, 2013, 51: 163-190.

[7] Cazzaniga S, Li ZR, Niyogi KK, Bassi R, Dall′Osto L. The Arabidopsis szl1 mutant reveals a critical role of b-carotene in photosystem I photoprotection. Plant Physiol, 2012, 159: 1745-1758.

[8] Chen Y, Liu T, Tian XH, Wang XF, Li M, Wang SX, Wang ZH. Effects of plastic film combined with straw mulch on grain yield and water use efficiency of winter wheat in Loess Plateau. Field Crop Res, 2015, 172(172): 53-58.

[9] Chen E, Zhang CM, Su YQ, Ma J, Zhang ZW, Yuan M, Zhang HY, Yuan S. Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat. Environ Exp Bot, 2017, 135(3): 45-55.

[10] Du KB, Xu L, Tu BK, Shen BX. Influences of soil flooding on ultrastructure and photosynthetic capacity of leaves of one-year old seedlings of two poplar clones. Scientia Silvae Sinica, 2010, 46(6): 58-64.

[11] Duan M, Feng HL, Wang LY, Li D, Meng QW. Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol, 2012, 169: 867-877.

[12] Falk J, Munné-Bosch S. Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot, 2010, 61: 1549-1566.

[13] Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol, 2011, 155: 93-100.

[14] Gameiro C, Utkin AB, Cartaxana P, Silva JMD, Matos AR. The use of laser induced chlorophyll fluorescence (LIF) as a fast and non–destructive method to investigate water deficit in Arabidopsis. Agric Water Manag, 2016, 164: 127-136.

[15] Gombos Z, Wada H, Murata AN. The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: A mechanism of chilling tolerance. Proc Natl Acad Sci, 2010, 91: 8787-8791.

[16] Gong B, Wen D, Vandenlangenberg K, Wei M, Wei M, Yang FJ, Shi QH, Wang XF. Comparative effects of NaCl and NaHCO₃, stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hortic, 2013, 157(3): 1-12.

[17] Gosling SN, Arnell NW. A global assessment of the impact of climate change on water scarcity. Clim Change, 2016, 134(3): 371-385.

[18] Govindjee G. Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol, 1995, 22: 131-160.

[19] Guo SJ, Zhou HY, Zhang XS, Li XG, Meng QW. Overexpression of CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J Plant Physiol, 2007, 164: 126-136.

[20] Haldimann P, Strasser RJ. Effects of anaerobiosis as probed by the polyphasic chlorophyll a fluorescence rise kinetic in pea (Pisum sativum L.). Photosynth Res, 1999, 62: 67-83.

[21] Hu YB, Sun GY, Wang XC. Induction characteristics and response of photosynthetic quantum conversion to changes in irradiance in mulberry plants. J Plant Physiol, 2007, 164(8): 959-968.

[22] Huang W, Zhang SB, Cao KF. The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res, 2010, 103: 175-182.

[23] Huppe HC, Turpin DH. Integration of carbon and nitrogen metabolism in plant and algal cells. Ann Rev Plant Physiol Plant Mol Biol, 1994, 45: 577-607.

[24] Jahnke LS, Hull MP, Long SP. Chilling stress and oxygen metabolizing enzymes in Zea diploperennis. Plant Cell Environ, 1991, 14: 97-104.

[25] Jiang CD, Jiang GM, Wang XZ, Li LH, Biswas DK, Li YG. Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP. Environ Exp Bot, 2006, 58(4): 261-268.

[26] Johnson GN. Reprint of: physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta, 2011, 1807: 906-911.

[27] Jung S, Steffen KL, Lee HJ. Comparative Photoinhibition of a high and a low altitude ecotype of tomato (Lycopersicon hirsutum) to chilling stress under high and light conditions. Plant Sci, 1998, 134: 69-77.

[28] Kreslavski VD, Carpentier R, Klimov VV, Murata N, Allakhverdiev SI. Molecular mechanisms of stress resistance of the photosynthetic apparatus. Biochem (Moscow) Suppl Ser A Membr Cell Biol, 2007, 1(3): 185-205.

[29] Li PM, Ma FW. Different effects of light irradiation on the photosynthetic electron transport chain during apple tree leaf dehydration. Plant Physiol Bioch, 2012, 55: 16-22.

[30] Li G, Gao HY, Zhao B, Dong ST, Zhang JW, Yang JS, Wang JF, Liu P. Effects of drought stress on activity of photosystems in leaves of maize at grain filling stage. Acta Agron sinica, 2009, 35(10): 1916-1922.

[31] Lyons JM. Chilling injury in plants. Ann Rev Plant Physiol, 1973, 24: 443-466.

[32] Malik AI, Colmer TD, Lambers H, Schortemeyer M. Changes in physiological and morphological traits of roots and shoots of wheat in response to different depths of waterlogging. Aust J Plant Physiol, 2001, 28(11): 1121-1131.

[33] Mathur S, Agrawal D, Jajoo A. Photosynthesis: response to high temperature stress. J Photochem Photobiol B, 2014, 137(8): 116-126.

[34] Müller P, Li XP, Niyogi KK. Non-photochemical quenching: a response to excess light energy. Plant Physiol, 2001, 125(4): 1558-1566.

[35] Nadia AA, Dewez D, Didur O, Popovic R. Inhibition of photosystem II photochemistry by Cr is caused by the alteration of both D1 protein and oxygen evolving complex. Photosynth Res, 2006, 89(89): 81-87.

[36] Nichols SN, Hofmann RW, Williams WM. Physiological drought resistance and accumulation of leaf phenolics in white clover interspecific hybrids. Environ Exp Bot, 2015, 119: 40-47.

[37] Oguchi R, Terashima I, Chow WS. The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. plants. Plant Cell Physiol, 2009, 50: 1815-1825.

[38] Omran RG, Benedict CR, Powell RG. effects of chilling on protein synthesis and CO₂ fixation in cotton leaves. Crop Sci, 1971, 11: 554-556.

[39] Qu NW, Zhou F, Gu ZJ, Jia SQ, Wang XA. Photosynthetic functions and chlorophyll fast fluorescence characteristics of five Pinus species. Chinese J Appl Ecol, 2012, 23(5): 1181-1187.

[40] Ravi I, Uma S, Vaganan MM, Mustaffa MM. Frontiers Phenotyping bananas for drought resistance. Plant Physiol, 2013, 4: 1-9.

[41] Russell AW, Critchley C, Robinson SA, Franklin LA, Seaton CCR, Chow WS, Anderson JM, Osmond CB. Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiol, 1992, 107: 943-952.

[42] Salmela MJ, Cavers S, Cottrell JE, lason GR, Ennos RA. Seasonal patterns of photochemical capacity and spring phenology reveal genetic differentiation among native Scots pine (Pinus sylvestris L.) populations in Scotland. For Ecol Manag, 2011, 262(6): 1020-1102.

[43] Satoh K, Fork DC. Photoinhibition of reaction centers of photosystems I and II in intact Bryopsis chloroplasts under anaerobic conditions. Plant Physiol, 1982, 70: 1004-1008.

[44] Scandalios GJ. Oxygen stress and superoxide dismutase. Plant Physiol, 1993, 101: 7-12.

[45] Sharma DK, Andersen SB, Ottosen CO, Rosenqvist E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol Plant, 2015, 153(2): 284-298.

[46] Shu DF, Wang LY, Duan M, Deng YS, Meng QW. Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress. Plant Physiol Bioch, 2011, 49: 1228-1237.

[47] Silvaa EN, Ferreira-Silvaa SL, Fontenelea ADV, Ribeirob RV, Viégasc RA, Silveiraa JAG. Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. J Plant Physiol, 2010, 167: 1157-1164.

[48] Spichalla JP, Desborogh SL. Superoxide dismutase, catalase, and α-tocopherol content of stored potato tubers. Plant Physiol, 1990, 94: 1214-1218.

[49] Strasser RJ, Srivastava A, Govindjee G. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol, 1995, 61(1): 32-42.

[50] Strasser RJ, Srivastava A, Govindjee G. Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res, 1997, 52(2): 147-155.

[51] Strauss AJ, Kruger GHJ, Strasser RJ, Heerden PDRV. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environ Exp Bot, 2006, 56(2): 147-157.

[52] Sun S, Wang SM, Wang JX, Gao HY. Effects of dehydration in the dark on functions of PS I and PS II in apricot (Prunus armeniaca L. ‘Jin Taiyang’) leaves. Acta Hortic Sinica, 2008, 35(1): 1-6.

[53] Takahashi M, Shigeto J, Sakamoto A, Morikawa H. Selective nitration of PsbO1, PsbO2, and PsbP1 decreases PSII oxygen evolution and photochemical efficiency in intact leaves of Arabidopsis. Plant Signal Behav, 2017 12 10 e1376157

[54] Taranishi Y, Tanaka A, Osumi Fukui S. Catalase activity of hydrocarbon utilizing Candida yeast. Agric Biol Chem, 1974, 38: 1213-1216.

[55] Troll W, Lindsey J. A photometric method for the determination of proline. J Biol Chem, 1955, 215: 655-660.

[56] Ushimaru T, Ogawa K, Ishida N, Shibasaka M, Kanematsu S, Asada K, Tsuji H. Changes in organelle superoxide dismutase isoenzymes during air adaptation of submerged rice seedlings: differential behavior of isoenzymes in plastids and mitochondoria. Planta, 1995, 196(3): 606-613.

[57] Wang BS, Luttg U, Ratajczak R. Effects of salt treatment and osmotic stress on V-ATPase and V-Pase in leaves of the halophyte Suaedasalsa. J Exp Bot, 2001, 52(365): 2355-2365.

[58] Wu H, Liu X, You L, Zhang LB, Zhou D, Feng JH, Zhao JM, Yu JB. Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in Halophyte Suaeda salsa. J Plant Growth Regul, 2012, 31(3): 332-341.

[59] Zhang LT, Gao HY, Zhang ZS, Xue ZC, Meng QW. Multiple effects of inhibition of mitochondrial alternative oxidase pathway on photosynthetic apparatus in Rumex K-1 leaves. Biol Plantarum, 2012, 56(2): 365-368.

[60] Zhang ZS, Li G, Gao HY, Liu P, Yang C, Meng XL, Meng QW. Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence, Zea mays L. Inbred Lines. Plos One, 2012 7 8 e42936

[61] Zhang HH, Zhong HX, Wang JF, Sui X, Xu N. Adaptive changes in chlorophyll content and photosynthetic features to low light in Physocarpus amurensis Maxim and Physocarpus opulifolius “Diabolo”. Peer J, 2016 4 3 e2125

[62] Zhang HH, Xu N, Li X, Jin WW, Tian Q, Gu SY, Sun GY. Overexpression of 2-Cys Prx increased salt tolerance of photosystem II (PSII) in tobacco. Int J Agric Biol, 2017, 19(4): 735-745.