Research Progress in the Mechanism of Plant Photosystem II（PSII）Responsing to Abiotic Stress

doi:10.13560/j.cnki.biotech.bull.1985.2023-0658

Abstract

Abstract:

Plant growth process is influenced by a series of abiotic stresses represented by environmental factors（temperature, drought, salinity, and heavy metals, etc.）, which hinder the photosynthetic process mainly characterized by substance conversion and energy metabolism. Photosystem II（PSII）is a multi-subunit pigment-protein complex located on the thylakoid membrane, which is particularly important for plant growth and development by capturing light energy to complete the photolysis of water and plastoquinone reduction. Generally, abiotic stress may inhibit the activity of PSII, affect its structure, and hinder electron transport and energy conversion. As the most vulnerable part of photosynthesis, PSII has attracted much attention in recent years due to its relationship with environmental factors. Based on this, this article summarized the physiological responses of plant PSII under major abiotic stresses such as temperature, drought, salt and heavy metals, and reviewed the structure and function of PSII, electron transfer process, photoinhibition and photoprotection based on chlorophyll fluorescence technology. It also provides a theoretical basis for further research on the physiological and molecular mechanisms of plant PSII response to abiotic stress.

Key words: abiotic stress, photosystem II（PSII）, chlorophyll fluorescence technique, photosynthetic electron transport, photoinhibition

CHENG Shuang, ULAANDUU Namuun, LI Zhuo-lin, HU Hai-ling, DENG Xiao-xia, LI Yue-ming, WANG Jing-hong, LIN Ji-xiang. Research Progress in the Mechanism of Plant Photosystem II（PSII）Responsing to Abiotic Stress[J]. Biotechnology Bulletin, 2023, 39(12): 33-42.

Figures/Tables 1

References 71

[1]	Sarkar T, Thankappan R, Mishra GP, et al. Advances in the development and use of DREB for improved abiotic stress tolerance in transgenic crop plants[J]. Physiol Mol Biol Plants, 2019, 25(6): 1323-1334. doi: 10.1007/s12298-019-00711-2
[2]	Landi M, Guidi L. Effects of abiotic stress on photosystem II proteins[J]. Photosynthetica, 2023, 61: 148-156. doi: 10.32615/ps.2022.043 URL
[3]	Zhang HH, Xu ZS, Huo YZ, et al. Overexpression of Trx CDSP32 gene promotes chlorophyll synthesis and photosynthetic electron transfer and alleviates cadmium-induced photoinhibition of PSII and PSI in tobacco leaves[J]. J Hazard Mater, 2020, 5(398): 122899.
[4]	Gupta R. The oxygen-evolving complex: a super catalyst for life on earth, in response to abiotic stresses[J]. Plant Signal Behav, 2020, 15(12): 1824721. doi: 10.1080/15592324.2020.1824721 URL
[5]	Huang W, Hu H, Zhang SB. Photorespiration plays an important role in the regulation of photosynthetic electron flow under fluctuating light in tobacco plants grown under full sunlight[J]. Front in Plant Sci, 2015, 6: 621.
[6]	Spetea C, Rintamäki E, Schoefs B. Changing the light environment: chloroplast signalling and response mechanisms[J]. Philos Trans R Soc Lond B Biol Sci, 2014, 369(1640): 20130220. doi: 10.1098/rstb.2013.0220 URL
[7]	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 pmid: 23913954
[8]	扆珩, 杨文强. 光合生物光抑制现象与光保护措施[J]. 植物生理学报, 2023, 59(4): 705-714.
	Yi H, Yang WQ. Photoinhibition and photoprotection of photosynthetic organisms[J]. Plant Physiol J, 2023, 59(4): 705-714.
[9]	原佳乐, 马超, 冯雅岚, 等. 不同抗旱性小麦快速叶绿素荧光诱导动力学曲线对干旱及复水的响应[J]. 植物生理学报, 2018, 54(6): 1119-1129.
	Yuan JL, Ma C, Feng YL, et al. Responses of rapid chlorophyll fluorescence induction kinetic curve of wheat with different drought resistance to drought stress and rehydration[J]. Plant Physiol J, 2018, 54(6): 1119-1129.
[10]	杨淑萍, 危常州, 梁永超. 盐胁迫对不同基因型海岛棉光合作用及荧光特性的影响[J]. 中国农业科学, 2010, 43(8): 1585-1593. doi: 10.3864/j.issn.0578-1752.2010.08.006
	Yang SP, Wei CZ, Liang YC. Effects of NaCl stress on the characteristics of photosynthesis and chlorophyll fluorescence at seedlings stage in different sea island cotton genotypes[J]. Sci Agric Sin, 2010, 43(8): 1585-1593.
[11]	朱春艳, 宋佳伟, 白天亮, 等. NaCl胁迫对不同耐盐性粳稻种质幼苗叶绿素荧光特性的影响[J]. 中国农业科学, 2022, 55(13): 2509-2525. doi: 10.3864/j.issn.0578-1752.2022.13.003
	Zhu CY, Song JW, Bai TL, et al. Effects of NaCl stress on the chlorophyll fluorescence characteristics of seedlings of Japonica rice germplasm with different salt tolerances[J]. Sci Agric Sin, 2022, 55(13): 2509-2525.
[12]	Xu HW, Lu Y, Tong SY. Effects of arbuscular mycorrhizal fungi on photosynthesis and chlorophyll fluorescence of maize seedlings under salt stress[J]. Emir J Food Agric, 2018: 199-204.
[13]	Rastogi A, Kovar M, He X, et al. JIP-test as a tool to identify salinity tolerance in sweet sorghum genotypes[J]. Photosynthetica, 2020, 58: 518-528. doi: 10.32615/ps.2019.169 URL
[14]	Hamdani S, Gauthier A, Msilini N, et al. Positive charges of polyamines protect PSII in isolated thylakoid membranes during photoinhibitory conditions[J]. Plant Cell Physiol, 2011, 52: 866-873. doi: 10.1093/pcp/pcr040 pmid: 21471122
[15]	Pérez-Bueno ML, Barón M, García -Luque I. PsbO, PsbP, and PsbQ of photosystem II are encoded by gene families in Nicotiana benthamiana. Structure and functionality of their isoforms[J]. Photosynthetica, 2011, 49(4): 573-580. doi: 10.1007/s11099-011-0070-7 URL
[16]	黄春雪. 甜菜叶绿素a-b结合蛋白基因BvLhcb-2的克隆与表达特性初步分析[D]. 哈尔滨: 黑龙江大学, 2022.
	Huang CX. Cloning and expression characteristics of chlorophyll a-b binding protein gene BvLhcb-2 in beet[D]. Harbin:Heilongjiang University, 2022.
[17]	逯久幸, 苗润田, 王司琦, 等. 低温胁迫下秋菊叶片光系统特性分析[J]. 植物生理学报, 2022, 58(2): 425-434.
	Lu JX, Miao RT, Wang SQ, et al. Analysis of photosystem features in autumn chrysanthemum leaves under low temperature stress[J]. Plant Physiol J, 2022, 58(2): 425-434.
[18]	Sharkey TD. Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene[J]. Plant, Cell Environ, 2005, 28(3): 269-277. doi: 10.1111/pce.2005.28.issue-3 URL
[19]	尹赜鹏, 鹿嘉智, 高振华, 等. 番茄幼苗叶片光合作用、PSII电子传递及活性氧对短期高温胁迫的响应[J]. 北方园艺, 2019(5): 1-11.
	Yin ZP, Lu JZ, Gao ZH, et al. Effects of photosynthetic, PSII electron transport and reactive oxygen species on short-term high temperature stress in tomato seedlings[J]. North Hortic, 2019(5): 1-11.
[20]	李书鑫, 徐婷, 李慧, 等. 低温胁迫对玉米幼苗叶绿素荧光诱导动力学的影响[J]. 土壤与作物, 2020, 9(3): 221-230.
	Li SX, Xu T, Li H, et al. Effects of low temperature on chlorophyll fluorescence kinetics of maize seedlings[J]. Soil Crop, 2020, 9(3): 221-230.
[21]	李岩宸, 杨再强, 杨立, 等. 苗期高温高湿条件对黄瓜叶片光系统 II中心叶绿素荧光特性的影响[J]. 中国农业气象, 2022, 43(11): 912-922.
	Li YC, Yang ZQ, Yang L, et al. Effects of high temperature and high humidity conditions at seedling stage on the chlorophyll fluorescence characteristics in the center of photosystem ii of cucumber leaves[J]. Chin J Agrometeorology, 2022, 43(11): 912-922.
[22]	Allakhverdiev SI, Murata N. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803[J]. Biochim Biophys Acta Bioenerg, 2004, 1657(1): 23-32. doi: 10.1016/j.bbabio.2004.03.003 URL
[23]	Murata N, Takahashi S, Nishiyama Y, et al. Photoinhibition of photosystem II under environmental stress[J]. Biochimi Biophys Acta Bioenerg, 2007, 1767(6): 414-421.
[24]	Li P, Zhu Y, Song X, et al. Negative effects of long-term moderate salinity and short-term drought stress on the photosynthetic performance of hybrid Pennisetum[J]. Plant Physiol Biochem, 2020, 155: 93-104. doi: 10.1016/j.plaphy.2020.06.033 URL
[25]	Nishiyama Y, Murata N. Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery[J]. Appl Microbiol Biotechnol, 2014, 98(21): 8777-8796. doi: 10.1007/s00253-014-6020-0 pmid: 25139449
[26]	Pandey J, Devadasu E, Saini D, et al. Reversible changes in structure and function of photosynthetic apparatus of pea(Pisum sativum)leaves under drought stress[J]. The Plant Journal, 2023, 113: 60-74. doi: 10.1111/tpj.v113.1 URL
[27]	Sárvári É, Mihailova G, Solti Á, et al. Comparison of thylakoid structure and organization in sun and shade Haberlea rhodopensis populations under desiccation and rehydration[J]. J Plant Physiol, 2014, 171(17): 1591-1600. doi: 10.1016/j.jplph.2014.07.015 URL
[28]	Sperdouli I, Moustakas M. Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress[J]. Acta Physiol Plant, 2012, 34(4): 1267-1276. doi: 10.1007/s11738-011-0920-8 URL
[29]	Liu WJ, Chen YE, Tian WJ, et al. Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress[J]. Biochim Biophys Acta Bioenerg, 2009, 1787(10): 1238-1245. doi: 10.1016/j.bbabio.2009.04.012 URL
[30]	Chen YE, Liu WJ, Su YQ, et al. Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana[J]. Physiol Plant, 2016, 158(2): 225-235.
[31]	Liu XJ, Zhang HH, Wang JR, et al. Increased CO₂concentrations increasing water use efficiency and improvement PSII function of mulberry seedling leaves under drought stress[J]. J Plant Interact, 2019, 14(1): 213-223. doi: 10.1080/17429145.2019.1603405 URL
[32]	Miao YY, Bi QR, Qin H, et al. Moderate drought followed by re-watering initiates beneficial changes in the photosynthesis, biomass production and Rubiaceae-type cyclopeptides(RAs)accumulation of Rubia yunnanensis[J]. Ind Crops Prod, 2020, 148: 112284. doi: 10.1016/j.indcrop.2020.112284 URL
[33]	Luo Y, Xie Y, He D, et al. Exogenous trehalose protects photosystem II by promoting cyclic electron flow under heat and drought stresses in winter wheat[J]. Plant Biol, 2021, 23(5): 770-776. doi: 10.1111/plb.v23.5 URL
[34]	陈彪, 张杰, 马晓寒, 等. 外源硒对干旱胁迫下烤烟叶绿素荧光特性和叶片化学成分的影响[J]. 中国农业科技导报, 2018, 20(10): 95-104. doi: 10.13304/j.nykjdb.2017.0666
	Chen B, Zhang J, Ma XH, et al. Influences of exogenous selenium on the chlorophyll fluorescence characteristics and chemical composition in flue-cured tobacco under drought stress[J]. J Agric Sci Technol, 2018, 20(10): 95-104.
[35]	孙欧文. 高温干旱胁迫对4个绣球品种生理生化特性的影响[D]. 杭州: 浙江农林大学, 2020.
	Sun OW. Effects of high temperature and drought stress on physiological and biochemical characteristics of four Hydrangea varieties[D]. Hangzhou: Zhejiang A&F University, 2020.
[36]	Zhao J, Yu WJ, Zhang LT, et al. Chlororespiration protects the photosynthetic apparatus against photoinhibition by alleviating inhibition of photodamaged-PSII repair in Haematococcus pluvialis at the green motile stage[J]. Algal Res, 2021, 54: 102140. doi: 10.1016/j.algal.2020.102140 URL
[37]	Liu X, Li LM, Li MJ, et al. AhGLK1 affects chlorophyll biosynthesis and photosynthesis in peanut leaves during recovery from drought[J]. Sci Rep, 2018, 8(1): 1-11.
[38]	Lambrev PH, Miloslavina Y, Jahns P, et al. On the relationship between non-photochemical quenching and photoprotection of Photosystem II[J]. Biochim Biophys Acta Bioenerg, 2012, 1817(5): 760-769. doi: 10.1016/j.bbabio.2012.02.002 URL
[39]	Ghosh D, Mohapatra S, Dogra V, et al. Improving photosynthetic efficiency by modulating non-photochemical quenching[J]. Trends Plant Sci, 2023, 28(3): 264-266. doi: 10.1016/j.tplants.2022.12.016 URL
[40]	Bano H, Athar HU, Zafar ZU, et al. Peroxidase activity and operation of photo-protective component of NPQ play key roles in drought tolerance of mung bean[Vigna radiata(L.) Wilcziek][J]. Physiol Plant, 2021, 172(2): 603-614.
[41]	Siddiqui MH, Alamri S, Alsubaie QD, et al. Melatonin and gibberellic acid promote growth and chlorophyll biosynthesis by regulating antioxidant and methylglyoxal detoxification system in tomato seedlings under salinity[J]. J Plant Growth Regul, 2020, 39(4): 1488-1502. doi: 10.1007/s00344-020-10122-3
[42]	张云鹤, 高大鹏, 王晓蕾, 等. 盐碱胁迫对水稻苗期光系统 II性能的影响[J]. 灌溉排水学报, 2022, 41(9): 52-60, 92.
	Zhang YH, Gao DP, Wang XL, et al. The effects of soil salinity on photosystem ii of rice seedlings[J]. J Irrigation Drainage, 2022, 41(9): 52-60, 92.
[43]	Mehta P, Jajoo A, Mathur S, et al. Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves[J]. Plant Physiol Biochem, 2010, 48(1): 16-20. doi: 10.1016/j.plaphy.2009.10.006 URL
[44]	Yin ZP, Lu JZ, Meng SD, et al. Exogenous melatonin improves salt tolerance in tomato by regulating photosynthetic electron flux and the ascorbate-glutathione cycle[J]. J Plant Interact, 2019, 14(1): 453-463. doi: 10.1080/17429145.2019.1645895 URL
[45]	Kalagi HM, Rastogi A, Zivcak M, et al. Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors[J]. Photosynthetica, 2018, 56(3): 953-961. doi: 10.1007/s11099-018-0766-z URL
[46]	Salim Akhter M, Noreen S, Mahmood S, et al. Influence of salinity stress on PSII in barley(Hordeum vulgare L.) genotypes, probed by chlorophyll-a fluorescence[J]. J King Saud Univ Sci, 2021, 33(1): 101239. doi: 10.1016/j.jksus.2020.101239 URL
[47]	周晓瑾, 黄海霞, 张君霞, 等. 盐胁迫对裸果木幼苗光合特性的影响[J]. 草业学报, 2023, 32(2): 75-83. doi: 10.11686/cyxb2022041
	Zhou XJ, Huang HX, Zhang JX, et al. Effects of salt stress on photosynthetic characteristics of Gymnocarpos przewalskii seedlings[J]. Acta Prataculturae sin, 2023, 32(2): 75-83.
[48]	刘晓龙, 徐晨, 徐克章, 等. 盐胁迫对水稻叶片光合作用和叶绿素荧光特性的影响[J]. 作物杂志, 2014(2): 88-92.
	Liu XL, Xu C, Xu KZ, et al. Effects on characteristics of photosynthesis and chlorophyll fluorescence of rice under salt stress[J]. Crops, 2014(2): 88-92.
[49]	Zhang HH, Li X, Che YH, et al. A study on the effects of salinity and pH on PSII function in mulberry seedling leaves under saline-alkali mixed stress[J]. Trees, 2020, 34(3): 693-706. doi: 10.1007/s00468-019-01949-9
[50]	Oukarroum A, Bussotti F, Goltsev V, et al. Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress[J]. Environ Exp Bot, 2015, 109: 80-88. doi: 10.1016/j.envexpbot.2014.08.005 URL
[51]	刘美岑, 张子健, 张东, 等. NaCl胁迫对甜瓜幼苗保护酶活性及光合性能的影响[J/OL]. 分子植物种, 2022. http://kns.cnki.net/kcms/detail/46.1068.S.20220926.1415.002.html.
	Liu MC, Zhang ZJ, Zhang D, et al. Effects of NaCl stress on protective enzyme activities and photosynthetic performance of muskmelon seedlings[J/OL]. Mol Plant Breed, 2022. http://kns.cnki.net/kcms/detail/46.1068.S.20220926.1415.002.html.
[52]	李焕勇, 廖方舟, 刘景超, 等. 盐胁迫对甜樱桃砧木生理特性及光合荧光参数的影响[J]. 西北植物学报, 2023, 43(1): 127-135.
	Li HY, Liao FZ, Liu JC, et al. Effect of salt stress on physiological characteristics and photosynthetic fluorescence parameters of sweet cherry rootstock[J]. Acta Bot Boreali-Occidentalia Sin, 2023, 43(1): 127-135.
[53]	Yang W, Dai H, Skuza L, et al. Enhanced Cd phytoextraction by Solanum nigrum L. from contaminated soils combined with the application of N fertilizers and double harvests[J]. Toxics, 2022, 10(5): 266. doi: 10.3390/toxics10050266 URL
[54]	Janik E, Maksymiec W, Mazur R, et al. Structural and functional modifications of the major light-harvesting complex ii in cadmium- or copper-treated secale cereale[J]. Plant Cell Physiol, 2010, 51(8): 1330-1340. doi: 10.1093/pcp/pcq093 pmid: 20627948
[55]	Chen YE, Mao HT, Wu N, et al. Different tolerance of photosynthetic apparatus to Cd stress in two rice cultivars with the same leaf Cd accumulation[J]. Acta Physiol Plant, 2019, 41(12): 1-13. doi: 10.1007/s11738-018-2785-6
[56]	Patra M, Bhowmik N, Bandopadhyay B, et al. Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance[J]. Environ Exp Bot, 2004, 52(3): 199-223. doi: 10.1016/j.envexpbot.2004.02.009 URL
[57]	Romanowska E, Wasilewska W, Fristedt R, et al. Phosphorylation of PSII proteins in maize thylakoids in the presence of Pb ions[J]. J Plant Physiol, 2012, 169(4): 345-352. doi: 10.1016/j.jplph.2011.10.006 URL
[58]	Xue ZC, Li JH, Li DS, et al. Bioaccumulation and photosynthetic activity response of sweet sorghum seedling(Sorghum bicolor L. Moench)to cadmium stress[J]. Photosynthetica, 2018, 56(4): 1422-1428. doi: 10.1007/s11099-018-0835-3 URL
[59]	邱岚, 何颀, 黄鑫浩, 等. 重金属铅对榉树幼树叶绿素荧光参数的影响[J]. 中南林业科技大学学报, 2018, 38(6): 123-129.
	Qiu L, He Q, Huang XH, et al. Response of chlorophyll fluorescence characteristic of Zelkova schneideriana sapling to Pb pollution[J]. J Central South Univ For Technol, 2018, 38(6): 123-129.
[60]	李陈贞, 孙亚莉, 刘红梅, 等. 镉胁迫下不同水稻品种幼苗生长及光合性能的差异[J]. 湖南农业大学学报: 自然科学版, 2021, 47(2): 147-152.
	Li CZ, Sun YL, Liu HM, et al. The difference of seedling growth and photosynthetic performance of different rice varieties under cadmium stress[J]. J Hunan Agric Univ Nat Sci, 2021, 47(2): 147-152.
[61]	于建军, 张贵龙, 黎娅, 等. 汞对烤烟光合作用和叶绿素荧光参数的影响[J]. 农业环境科学学报, 2008, 27(5): 1963-1968.
	Yu JJ, Zhang GL, Li Y, et al. Effects of mercury on photosynthesis and chlorophyll fluorescence parameters of flue-cured tobacco[J]. J Agro Environ Sci, 2008, 27(5): 1963-1968.
[62]	Chen HZ, Song LL, Zhang HB, et al. Cu and Zn stress affect the photosynthetic and antioxidative systems of alfalfa(Medicago sativa)[J]. J Plant Interact, 2022, 17(1): 695-704. doi: 10.1080/17429145.2022.2074157 URL
[63]	Zhang HH, Li X, Xu ZS, et al. Toxic effects of heavy metals Pb and Cd on mulberry(Morus alba L.)seedling leaves: Photosynthetic function and reactive oxygen species(ROS)metabolism responses[J]. Ecotoxicol Environ Saf, 2020, 195: 110469. doi: 10.1016/j.ecoenv.2020.110469 URL
[64]	姚广, 高辉远, 王未未, 等. 铅胁迫对玉米幼苗叶片光系统功能及光合作用的影响[J]. 生态学报, 2009, 29(3): 1162-1169.
	Yao G, Gao HY, Wang WW, et al. The effects of Pb-stress on functions of photosystems and photosynthetic rate in maize seedling leaves[J]. Acta Ecol Sin, 2009, 29(3): 1162-1169.
[65]	杨富文. 重金属镉和锌抑制烟草光合作用及活性氧代谢的功能研究[D]. 哈尔滨: 东北林业大学, 2022.
	Yang FW. Study on the function of cadmium and zinc in inhibiting tobacco photosynthesis and reactive oxygen species metabolism[D]. Harbin:Northeast Forestry University, 2022.
[66]	朱凡, 雷佳奇, 黄鑫浩, 等. 木本植物光反应对重金属胁迫响应机制的研究进展[J]. 中南林业科技大学学报, 2022, 42(10): 9-21.
	Zhu F, Lei JQ, Huang XH, et al. Advances in response mechanism of the light reaction of woody plants to heavy metal stress[J]. J Central South Univ For Technol, 2022, 42(10): 9-21.
[67]	Shi Y, Che Y, Wang Y, et al. Loss of mature D1 leads to compromised CP43 assembly in Arabidopsis thaliana[J]. BMC Plant Biol, 2021, 21(1): 106. doi: 10.1186/s12870-021-02888-9
[68]	陈茹, 朱丽, 侯昕. 类囊体膜对光胁迫的适应机制[J]. 生物学杂志, 2021, 38(1): 88-92.
	Chen R, Zhu L, Hou X. The mechanism of thylakoid membrane adapting to light stress[J]. J Biol, 2021, 38(1): 88-92.
[69]	梁英, 李玉婷, 车兴凯, 等. 小麦叶片PSI光抑制对光合电子传递链的影响[J]. 植物生理学报, 2018, 54(9): 1426-1432.
	Liang Y, Li YT, Che XK, et al. Effects of PSI Photoinhibition on photosynthetic electron transports chain in wheat(Triticum aestivum)leaves[J]. Plant Physiol J, 2018, 54(9): 1426-1432.
[70]	Yang YJ, Zhang SB, Huang W. Photosynthetic regulation under fluctuating light in young and mature leaves of the CAM plant Bryophyllum pinnatum[J]. Biochim Biophys Acta Bioenerg, 2019, 1860(6): 469-477. doi: 10.1016/j.bbabio.2019.04.006 URL
[71]	Takagi D, Takumi S, Hashiguchi M, et al. Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem i photoinhibition[J]. Plant Physiol, 2016, 171(3): 1626-1634. doi: 10.1104/pp.16.00246 pmid: 26936894