Effects of cold stress on leaf physiological characteristics in <i>Forsythia suspensa</i> (Thunb.) Vahl seedlings

Li Yong; Wang Fan; Wang Shu-Chen; Yang Ya-Lin; Zhang Ling

doi:10.11913/PSJ.2095-0837.22091

Plant Science Journal > 2023 > 41(1): 102-111. > DOI: 10.11913/PSJ.2095-0837.22091 CSTR: 32231.14.PSJ.2095-0837.22091

Li Y，Wang F，Wang SC，Yang YL，Zhang L. Effects of cold stress on leaf physiological characteristics in Forsythia suspensa (Thunb.) Vahl seedlings[J]. Plant Science Journal，2023，41（1）：102−111. DOI: 10.11913/PSJ.2095-0837.22091

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Effects of cold stress on leaf physiological characteristics in Forsythia suspensa (Thunb.) Vahl seedlings

1.
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou 450002, China
2.
College of Forestry, Henan Agricultural University, Zhengzhou 450002, China

Funds: This work was supported by a grant from the National Natural Science Foundation of China (31770225)

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Received Date: July 14, 2022
Revised Date: September 02, 2022
Available Online: March 02, 2023

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Abstract

Abstract

Forsythia suspensa (Thunb.) Vahl is a common early spring flower and bulk cultivated medicinal crop. Low temperature is the main stress factor for this species in spring. To date, however, no physiological research has explored the effects of low temperature on F. suspensa growth. Here, we used the leaves of F. suspensa seedlings and detected changes in relative conductivity, malondialdehyde (MDA), proline content (Pro), soluble sugar (SS), soluble protein (SP), chlorophyll content, superoxide dismutase (SOD), peroxidase (POD) activity, and chlorophyll fluorescence parameters under four temperature conditions. We also detected chlorophyll fluorescence parameters after recovery. Results showed that low temperature stress caused an increase in relative electrical conductivity and MDA content in the leaves, which affected growth to some extent. The resistance of F. suspensa leaves to low temperature was achieved by multiple pathways. SP, SS, and SOD played major roles at the early stage of cold stress, while Pro and POD played important roles when stress intensity increased. The JIP-test showed that low temperature had a significant effect on photosynthesis, mainly reflected in the inhibition of electron transfer and damage to the receptor side. Treatment damage at 0℃ was the most serious. Low temperature stress affected the growth of F. suspensa seedlings. Low temperature stress above 4℃ affected the seedlings, but growth recovered after the stress was removed. Damage caused by low temperature stress at 0℃ was irreversible. Thus, F. suspensa should be cultivated in areas where low temperatures are less common in late spring, or cold-tolerant varieties should be selected for cultivation in areas where low temperatures are more frequent in late spring.
- Forsythia suspense,
- Cold stress,
- Photosynthesis,
- JIP-test,
- Chlorophyll fluorescence

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[1]	Gao JP,Wallis JG,Jewell JB,Browse J. Trimethylguanosine synthase1 (TGS1) is essential for chilling tolerance[J]. Plant Physiol,2017,174 (3):1713−1727. doi: 10.1104/pp.17.00340
[2]	张晓虎. 洛南县连翘产地气候因素分析研究[J]. 陕西农业科学,2018,64(9):25−29. doi: 10.3969/j.issn.0488-5368.2018.09.009
[3]	Wu DX,Kukkonen S,Luoranen J,Pulkkinen P,Repo T,et al. Influence of late autumn preconditioning temperature on frost hardiness of apple,blueberry and blackcurrant saplings[J]. Sci Hortic,2019,258:108755. doi: 10.1016/j.scienta.2019.108755
[4]	Nejadsadeghi L,Maali-Amiri R,Zeinali H,Ramezanpour S,Sadeghzade B. Membrane fatty acid compositions and cold-induced responses in tetraploid and hexaploid wheats[J]. Mol Biol Rep,2015,42 (2):363−372. doi: 10.1007/s11033-014-3776-3
[5]	Gill SS,Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants[J]. Plant Physiol Biochem,2010,48 (12):909−930. doi: 10.1016/j.plaphy.2010.08.016
[6]	Yang QS,Wu JH,Li CY,Wei YR,Sheng O,et al. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB group) seedlings[J]. Mol Cell Proteomics,2012,11 (12):1853−1869. doi: 10.1074/mcp.M112.022079
[7]	Xu J,Li Y,Sun J,Du L,Zhang Y. Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance[J]. Plant Biol,2013,15 (2):292−303. doi: 10.1111/j.1438-8677.2012.00639.x
[8]	Jin JJ,Zhang H,Zhang JF,Liu PP,Chen X,et al. Integrated transcriptomics and metabolomics analysis to characterize cold stress responses in Nicotiana tabacum[J]. BMC Genomics,2017,18 (1):496. doi: 10.1186/s12864-017-3871-7
[9]	Gothandam KM,Nalini E,Karthikeyan S,Shin JS. OsPRP3,a flower specific proline-rich protein of rice,determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance[J]. Plant Mol Biol,2010,72 (1-2):125−135. doi: 10.1007/s11103-009-9557-z
[10]	Yang Y,Yao N,Jia ZK,Jia J,Duan FJ,et al. Effect of exogenous abscisic acid on cold acclimation in two Magnolia species[J]. Biol Plant,2016,60 (3):555−562. doi: 10.1007/s10535-016-0623-5
[11]	Thakur P,Kumar S,Malik JA,Berger JD,Nayyar H. Cold stress effects on reproductive development in grain crops:an overview[J]. Environ Exp Bot,2010,67 (3):429−443. doi: 10.1016/j.envexpbot.2009.09.004
[12]	Ensminger I,Busch F,Huner NPA. Photostasis and cold acclimation:sensing low temperature through photosynthesis[J]. Physiol Plant,2006,126 (1):28−44. doi: 10.1111/j.1399-3054.2006.00627.x
[13]	Kong FY,Deng YS,Zhou B,Wang GD,Wang Y,Meng QW. A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem Ⅱ under chilling stress[J]. J Exp Bot,2014,65 (1):143−158. doi: 10.1093/jxb/ert357
[14]	Wang ZY,Xia Q,Liu X,Liu WX,Huang WZ,et al. Phytochemistry,pharmacology,quality control and future research of Forsythia suspensa (Thunb.) Vahl:a review[J]. J Ethnopharmacol,2018,210:318−339. doi: 10.1016/j.jep.2017.08.040
[15]	Li C,Wei Q,Zou ZH,Sun CZ,Wang Q,et al. A lignan and a lignan derivative from the fruit of Forsythia suspensa[J]. Phytochem Lett,2019,32:115−118. doi: 10.1016/j.phytol.2019.05.009
[16]	Heath RL,Packer L. Photoperoxidation in isolated chloroplast:Ⅰ. Kinetics and stoichiometry of fatty acid peroxidation[J]. Arch Biochem Biophys,1968,125 (1):189−198. doi: 10.1016/0003-9861(68)90654-1
[17]	王永军,杨今胜,袁翠平,柳京国,李登海,董树亭. 超高产夏玉米花粒期不同部位叶片衰老与抗氧化酶特性[J]. 作物学报,2013,39(12):2183−2191. Wang YJ,Yang JS,Yuan CP,Liu JG,Li DH,Dong ST. Characteristics of senescence and antioxidant enzyme activities in leaves at different plant parts of summer maize with the super-high yielding potential after anthesis[J]. Acta Agronomica Sinica,2013,39 (12):2183−2191. doi: 10.3724/SP.J.1006.2013.02183 Wang YJ, Yang JS, Yuan CP, Liu JG, Li DH, Dong ST. Characteristics of senescence and antioxidant enzyme activities in leaves at different plant parts of summer maize with the super-high yielding potential after anthesis[J]. Acta Agronomica Sinica, 2013, 39（12）: 2183-2191. doi: 10.3724/SP.J.1006.2013.02183
[18]	Redmann RE,Haraldson J,Gusta LV. Leakage of UV-absorbing substances as a measure of salt injury in leaf tissue of woody species[J]. Physiol Plant,1986,67 (1):87−91. doi: 10.1111/j.1399-3054.1986.tb01267.x
[19]	Lichtenthaler HK,Wellburn AR. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents[J]. Biochem Soc Trans,1983,11 (5):591−592. doi: 10.1042/bst0110591
[20]	Rosa M,Hilal M,González JA,Prado FE. Low-temperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings[J]. Plant Physiol Biochem,2009,47 (4):300−307. doi: 10.1016/j.plaphy.2008.12.001
[21]	Bates LS,Waldren RP,Teare ID. Rapid determination of free proline for water-stress studies[J]. Plant Soil,1973,39 (1):205−207. doi: 10.1007/BF00018060
[22]	Haldimann P,Strasser RJ. Effects of anaerobiosis as probed by the polyphasic chlorophyll a fluorescence rise kinetic in pea (Pisum sativum L. )[J]. Photosyn Res,1999,62 (1):67−83. doi: 10.1023/A:1006321126009
[23]	Strasser RJ,Tsimilli-Michael M,Qiang S,Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis[J]. Biochim Biophys Acta Bioenerg,2010,1797 (6-7):1313−1326. doi: 10.1016/j.bbabio.2010.03.008
[24]	Arslan Ö,Eyidoğan F,Ekmekçi Y. Freezing tolerance of chickpea:biochemical and molecular changes at vegetative stage[J]. Biol Plant,2018,62 (1):140−148. doi: 10.1007/s10535-017-0760-5
[25]	Lukatkin AS,Brazaitytė A,Bobinas C,Duchovskis P. Chilling injury in chilling-sensitive plants:a review[J]. Zemdirbyste,2012,99 (2):111−124.
[26]	程祥飞,王磊,聂林杰,李永华. 低温胁迫下菊花叶片叶绿素荧光特性与抗氧化酶活性的变化[J]. 河南农业科学,2018,47(4):104−108. Cheng XF,Wang L,Nie LJ,Li YH. Chlorophyll fluorescence characteristics and antioxidant enzyme activities of chrysanthemum leaves under low temperature stress[J]. Journal of Henan Agricultural Sciences,2018,47 (4):104−108. Cheng XF, Wang L, Nie LJ, Li YH. Chlorophyll fluorescence characteristics and antioxidant enzyme activities of chrysanthemum leaves under low temperature stress[J]. Journal of Henan Agricultural Sciences, 2018, 47（4）: 104-108.
[27]	Fu ZZ,Lei YK,Peng DD,Li Y. Population genetics of the widespread shrub Forsythia suspensa (Oleaceae) in warm-temperate China using microsatellite loci:implication for conservation[J]. Plant Syst Evol,2016,302 (1):1−9. doi: 10.1007/s00606-015-1241-y
[28]	李清亚,路斌,赵佳伟,栗浩,李艳,等. 不同豆梨品种对低温胁迫的生理响应及抗寒性评价[J]. 西北农林科技大学学报(自然科学版),2020,48(1):86−94,110. Li QY,Lu B,Zhao JW,Li H,Li Y,et al. Physiological response and cold resistance evaluation of different Pyrus calleryan varieties under low temperature stress[J]. Journal of Northwest A & F University (Natural Science Edition),2020,48 (1):86−94,110. Li QY, Lu B, Zhao JW, Li H, Li Y, et al. Physiological response and cold resistance evaluation of different Pyrus calleryan varieties under low temperature stress[J]. Journal of Northwest A & F University （Natural Science Edition）, 2020, 48（1）: 86-94, 110.
[29]	Zhang Q,Liu YX,Yu QQ,Ma Y,Gu WR,Yang DG. Physiological changes associated with enhanced cold resistance during maize (Zea mays) germination and seedling growth in response to exogenous calcium[J]. Crop Pasture Sci,2020,71 (6):529−538. doi: 10.1071/CP19510
[30]	Feng Q,Yang S,Wang YJ,Lu L,Sun MT,et al. Physiological and molecular mechanisms of ABA and CaCl₂ regulating chilling tolerance of cucumber seedlings[J]. Plants,2021,10 (12):2746. doi: 10.3390/plants10122746
[31]	Ignatenko A,Talanova V,Repkina N,Titov A. Exogenous salicylic acid treatment induces cold tolerance in wheat through promotion of antioxidant enzyme activity and proline accumulation[J]. Acta Physiol Plant,2019,41 (6):80. doi: 10.1007/s11738-019-2872-3
[32]	Wang SQ,Zhao HH,Zhao LM,Gu CM,Na YG,Scholes GD. Application of brassinolide alleviates cold stress at the booting stage of rice[J]. J Integr Agric,2020,19 (4):975−987. doi: 10.1016/S2095-3119(19)62639-0
[33]	Mirkovic T,Ostroumov EE,Anna JM,van Grondelle R,Govindjee,et al. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms[J]. Chem Rev,2017,117 (2):249−293. doi: 10.1021/acs.chemrev.6b00002
[34]	Borawska-Jarmułowicz B,Mastalerczuk G,Kalaji HM,Carpentier R,Pietkiewicz S,Allakhverdiev SI. Photosynthetic efficiency and survival of Dactylis glomerata and Lolium perenne following low temperature stress[J]. Russ J Plant Physiol,2014,61 (3):281−288. doi: 10.1134/S1021443714030029
[35]	Gururani MA,Venkatesh J,Tran LSP. Regulation of photosynthesis during abiotic stress-induced photoinhibition[J]. Mol Plant,2015,8 (9):1304−1320. doi: 10.1016/j.molp.2015.05.005
[36]	Guisse B,Srivastava A,Strasser R. The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves[J]. Arch Sci,1995,48 (2):147−160.
[37]	Kalaji HM,Jajoo A,Oukarroum A,Brestic M,Zivcak M,et al. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions[J]. Acta Physiol Plant,2016,38 (4):102. doi: 10.1007/s11738-016-2113-y
[38]	Murchie EH,Lawson T. Chlorophyll fluorescence analysis:a guide to good practice and understanding some new applications[J]. J Exp Bot,2013,64 (13):3983−3998. doi: 10.1093/jxb/ert208
[39]	Zhou R,Wu Z,Wang X,Rosenqvist E,Wang YL,et al. Evaluation of temperature stress tolerance in cultivated and wild tomatoes using photosynthesis and chlorophyll fluorescence[J]. Hortic Environ Biotechnol,2018,59 (4):499−509. doi: 10.1007/s13580-018-0050-y
[40]	Lee HY,Hong YN,Chow WS. Photoinactivation of photosystem Ⅱ complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves[J]. Planta,2001,212 (3):332−342. doi: 10.1007/s004250000398
[41]	Guha A,Sengupta D,Reddy AR. Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought[J]. J Photochem Photobiol B,2013,119:71−83. doi: 10.1016/j.jphotobiol.2012.12.006
[42]	曲丽娜,许楠,张会慧. 风箱果和紫叶风箱果叶片光系统Ⅱ功能对秋季低温的响应[J]. 东北林业大学学报,2018,46(8):42−48. Qu LN,Xu N,Zhang HH. Response of photosynthetic function of photosystem Ⅱ in leaves of Physocarpus amurensis maxim and P. opulifolius in autumn low temperature stress in cold regions[J]. Journal of Northeast Forestry University,2018,46 (8):42−48. Qu LN, Xu N, Zhang HH. Response of photosynthetic function of photosystem II in leaves of Physocarpus amurensis maxim and P. opulifolius in autumn low temperature stress in cold regions[J]. Journal of Northeast Forestry University, 2018, 46（8）: 42-48.
[43]	Maliba BG,Inbaraj PM,Berner JM. The effect of ozone and drought on the photosynthetic performance of canola[J]. J Integr Agric,2018,17 (5):1137−1144. doi: 10.1016/S2095-3119(17)61834-3
[44]	Roháček K. Chlorophyll fluorescence parameters:the definitions,photosynthetic meaning,and mutual relationships[J]. Photosynthetica,2002,40 (1):13−29. doi: 10.1023/A:1020125719386
[45]	Snider JL,Thangthong N,Pilon C,Virk G,Tishchenko V. OJIP-fluorescence parameters as rapid indicators of cotton (Gossypium hirsutum L. ) seedling vigor under contrasting growth temperature regimes[J]. Plant Physiol Biochem,2018,132:249−257. doi: 10.1016/j.plaphy.2018.09.015

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Effects of cold stress on leaf physiological characteristics in Forsythia suspensa (Thunb.) Vahl seedlings