Abstract
Photosystem II (PSII), especially the D1 protein, is highly sensitive to the detrimental impact of heat stress. Photoinhibition always occurs when the rate of photodamage exceeds the rate of D1 protein repair. Here, genetically engineered codA-tomato with the capability to accumulate glycinebetaine (GB) was established. After photoinhibition treatment at high temperature, the transgenic lines displayed more thermotolerance to heat-induced photoinhibition than the control line. GB maintained high expression of LeFtsHs and LeDegs and degraded the damaged D1 protein in time. Meanwhile, the increased transcription of synthesis-related genes accelerated the de novo synthesis of D1 protein. Low ROS accumulation reduced the inhibition of D1 protein translation in the transgenic plants, thereby reducing protein damage. The increased D1 protein content and decreased phosphorylated D1 protein (pD1) in the transgenic plants compared with control plants imply that GB may minimize photodamage and maximize D1 protein stability. As D1 protein exhibits a high turnover, PSII maybe repaired rapidly and efficiently in transgenic plants under photoinhibition treatment at high temperature, with the resultant mitigation of photoinhibition of PSII.
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Ahammed GJ, Li X, Yang YX, Liu CC, Zhou GZ, Wang HJ, Cheng Y (2019) Tomato WRKY81 acts as a negative regulator for drought tolerance by modulating guard cell H2O2–mediated stomatal closure. Environ Exp Bot 171:103960
Ahammed GJ, Li X, Wan HJ, Zhou GZ, Cheng Y (2020) SlWRKY81 reduces drought tolerance by attenuating proline biosynthesis in tomato. Sci Hortic 270:109444
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 303:161–175
Ahmad P, Latef AA, Hashem A, Allah EF, Gucel S, Tran LP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in Chickpea. Front Plant Sci 7:347–347
Ahmad P, Tripathi DK, Deshmukh R, Singh VP, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environ Exp Bot 161:1–3
Alia HH, Sakamoto A, Murata N (1998) Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J 16:155–161
Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp PCC 6803. Biochim Biophys Acta 1657:23–32
Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550
Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P (2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Front in Plant Sci 10:230
Aro EM, Kettunen R, Tyystjrvi E (1992) ATP and light regulate D1 protein modification and degradation Role of D1* in photoinhibition. FEBS Lett 297:29–33
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
Aryal BP, Jeong J, Rao VA (2015) Abstract 1825: carbonylation and degradation of cardiac myosin binding protein C serves as an indicator of doxorubicin-induced cardiotoxicity. Cancer Res 75:1825–1825
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
Barta C, Dunkle AM, Wachter RM, Salvucci ME (2010) Structural changes associated with the acute thermal instability of Rubisco activase. Arch Biochem Biophys 499:17–25
Basha E, Lee GJ, Breci LA, Hausrath AC, Buan NR, Giese KC, Vierling E (2004) The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J Biol Chem 279:7566–7575
Basha E, Jones C, Wysocki V, Vierling E (2010) Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J Biol Chem 285:11489–11497
Bohnert HJ, Jensen RG (1996) Strategies for engineering water-stress tolerance in plants. Trends Biotechnol 14:89–97
Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416
Cao P, Su X, Pan X, Liu Z, Chang W, Li M (2018) Structure, assembly and energy transfer of plant photosystem II supercomplex. Biochim Biophys Acta 1859:633–644
Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257
Chen THH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505
Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20
Chen LB, Jia HY, Tian Q, Du LB, Gao YL, Miao XX, Liu Y (2012) Protecting effect of phosphorylation on oxidative damage of D1 protein by down-regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Res 112:141–148
Chen Y, Zhang CM, Su YQ, Ma J, Zhang ZW, Yuan M, Zhang HY, Yuan S (2017) Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat. Environ Exp Bot 135:45–55
Deshnium P, Los DA, Hayashi H, Mustardy L, Murata N (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–907
Dou H, Xv K, Meng QW, Li G, Yang XH (2015) Potato plants ectopically expressing Arabidopsis thaliana CBF3 exhibit enhanced tolerance to high-temperature stress. Plant Cell Environ 38:61–72
Dwivedi SK, Basu S, Kumar S, Kumari S, Kumar A, Jha S, Mishra JS, Bhatt BP, Kumar G (2019) Enhanced antioxidant enzyme activities in developing anther contributes to heat stress alleviation and sustains grain yield in wheat. Funct Plant Biol 46:1090–1102
Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620
Fagerlund RD, Forsman JA, Biswas S, Vass I, Davies FK, Summerfield TC, Eaton-Rye JJ (2020) Stabilization of Photosystem II by the PsbT protein impacts photodamage, repair and biogenesis. Biochim Biophys Acta Bioenerg 1861:148234
Fristedt R, Willig A, Granath P, Crèvecoeur M, Rochaix JD, Vener AV (2009) Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21:3950–3964
Gao YB, Zheng WW, Zhang C, Zhang LL, Xu K (2019) High temperature and high light intensity induced photoinhibition of bayberry (Myricarubra Sieb. et Zucc.) by disruption of D1 turnover in photosystem II. Sci Hortic 248:132–137
Gerganova MT, Faik AK, Velitchkova MY (2019) Acquired tolerance of the photosynthetic apparatus to photoinhibition as a result of growing Solanumlycopersicum at moderately higher temperature and light intensity. Funct Plant Biol 46:555–566
Gerotto C, Trotta A, Bajwa AA, Mancini I, Morosinotto T, Aro EM (2019) Thylakoid protein phosphorylation dynamics in a moss mutant lacking serine/threonine protein kinase STN8. Plant Physiol 180:1582–1597
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314
González BE, Barbato R, Aro EM (1999) Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta 208:196–204
Huang S, Zuo T, Ni WZ (2020) Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses. Planta 251:36
Jajoo A, Szabó M, Zsiros O, Garab G (2012) Low pH induced structural reorganization in thylakoid membranes. Biochim Biophys Acta 1817:1388–1391
Jimbo H, Yutthanasirikul R, Nagano T, Hisabori T, Hihara Y, Nishiyama Y (2018) Oxidation of translation factor EF-Tu inhibits the repair of photosystem II. Plant Physiol 176:2691–2699
Jimbo H, Izuhara T, Hihara Y, Hisabori T, Nishiyama Y (2019) Light-inducible expression of translation factor EF-Tu during acclimation to strong light enhances the repair of photosystem II. Proc Natl Acad Sci USA 116:21268–21273
Jin H, Fu M, Duan Z, Duan S, Li M, Dong X, Liu B, Feng D, Wang J, Peng L, Wang HB (2018) LOW PHOTOSYNTHETIC EFFICIENCY 1 is required for light-regulated photosystem II biogenesis in Arabidopsis. Proc Natl Acad Sci USA 115:E6075–E6084
Kale R, Hebert AE, Frankel LK, Sallans L, Bricker TM, Pospíšil P (2017) Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II. Proc Natl Acad Sci USA 114:2988–2993
Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of PSII from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047
Kato Y, Sakamoto W (2014) Phosphorylation of photosystem II core proteins prevents undesirable cleavage of D1 and contributes to the fine-tuned repair of photosystem II. Plant J 79:312–321
Kato Y, Miura E, Ido K, Sakamoto W (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol 151:1790–1801
Kato Y, Ozawa S, Takahashi Y, Sakamoto W (2015) D1 fragmentation in photosystem II repair caused by photo-damage of a two-step model. Photosynth Res 126:409–416
Kato Y, Hyodo K, Sakamoto W (2018) The photosystem II repair cycle requires FtsH turnover through the EngA GTPase. Plant Physiol 178:596–611
Kaur H, Sirhindi H, Bhardwaj R, Alyemeni MN, Siddique KHM, Ahmad P (2018) 28-homobrassinolide regulates antioxidant enzyme activities and gene expression in response to salt- and temperature-induced oxidative stress in Brassicajuncea. Sci Rep 8:8735
Kirchhoff H (2013) Structural constraints for protein repair in plant photosynthetic membranes. Plant Signal Behav 8:e23634
Koivuniemi A, Aro EM, Andersson B (1995) Degradation of the D1- and D2- proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34:16022–16029
Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, Hayashi H, Nishiyama Y (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol 65:936–947
Kojima K, Motohashi K, Morota T, Oshita M, Hisabori T, Hayashi H, Nishiyama Y (2009) Regulation of translation by the redox state of elongation factor G in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 284:18685–18691
Komayama K, Khatoon M, Takenaka D, Horie J, Yamashita A, Yoshioka M, Nakayama Y, Yoshida M, Ohira S, Morita N, Velitchkova M, Enami I, Yamamoto Y (2007) Quality control of photosystem II: cleavage and aggregation of heat-damaged D1 protein in spinach thylakoids. Biochim Biophys Acta 1767:838–846
Kong FY, Deng Y, Zhou B, Wang GD, Wang Y, Meng QW (2014) A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress. J Exp Bot 65:143–158
Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Hüner NP (2015) Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 126:221–235
Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122:189–198
Li SF, Li F, Wang JW, Zhang W, Meng QW, Chen THH, Murata N, Yang XH (2011) Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant Cell Environ 34:1931–1943
Li MF, Li ZM, Li SF, Guo SJ, Meng QW, Li G, Yang XH (2014) Genetic engineering of glycine betaine biosynthesis reduces heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Mol Biol Rep 32:42–51
Li DX, Zhang TP, Wang MW, Liu Y, Brestic M, Chen TH, Yang XH (2018) Genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato. Front Plant Sci 9:1995
Liu Y, Wang L, Jiang SS, Pan JW, Cai GH, Li DQ (2014) Group 5 LEA protein, ZmLEA5C, enhance tolerance to osmotic and low temperature stresses in transgenic tobacco and yeast. Plant Physiol Biochem 84:22–31
Liu Y, Song QP, Li DX, Yang XH, Li DQ (2017) Multifunctional roles of plant dehydrins in response to environmental stresses. Front Plant Sci 8:1018
Liu J, Lu Y, Hua W, Last RL (2019) A new light on Photosystem II maintenance in oxygenic photosynthesis. Front Plant Sci 10:975
Löw D, Brändle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211:575–582
Lu Y (2016) Identification and roles of photosystem II assembly, stability, and repair factors in Arabidopsis. Front Plant Sci 7:168
Masood A, Per TS, Asgher M, Fatma M, Khan MIR, Rasheed F, Hussain SJ, Khan NA (2016) Glycine betaine: role in shifting plants toward adaptation under extreme environments. Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, New Delhi, pp 69–82
Mccue KF, Hanson AD (1990) Drought and salt tolerance: towards understanding and application. Trends Biotechnol 8:358–362
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta 1817:247–257
Murata N, Nishiyama Y (2018) ATP is a driving force in the repair of photosystem II during photoinhibition. Plant Cell Environ 41:285–299
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92
Nagano T, Kojima K, Hisabori T, Hayashi H, MoritaEH KT, Miyagi T, Ueda T, Nishiyama Y (2012) Elongation factor G is a critical target during oxidative damage to the translation system of Escherichia coli. J Biol Chem 287:28697–28704
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nath K, Poudyal RS, Eom JS, Park YS, Zulfugarov IS, Mishra SR, Tovuu A, Ryoo N, Yoon HS, Nam HG, An G, Jeon JS, Lee CH (2013) Loss-of-function of OsSTN8 suppresses the photosystem II core protein phosphorylation and interferes with the photosystem II repair mechanism in rice (Oryza sativa). Plant J 76:675–686
Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biot 98:8777–8796
Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594
Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16
Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiol 141:758–765
Park EJ, Jeknić Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen THH (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 40:474–487
Park EJ, Jeknić Z, Pino MT, Murata N, Chen THH (2007) Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005
Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807:887–896
Poudyal RS, Nath K, Zulfugarov IS, Lee CH (2016) Production of superoxide from photosystem II-light harvesting complex II supercomplex in STN8 kinase knock-out rice mutants under photoinhibitory illumination. J Photochem Photobiol B 162:240–247
Poudyal D, Rosenqvist E, Ottosen CO (2019) Phenotyping from lab to field - tomato lines screened for heat stress using Fv/Fm maintain high fruit yield during thermal stress in the field. Funct Plant Biol 46:44–55
Prasad PVV, Pisipati SR, Mutava RN, Tuinstra MR (2008) Sensitivity of grain sorghum to high temperature stress during reproductive development. Crop Sci 48:1911–1917
Prasad PVV, Vu JCV, Boote KJ, Allen LH (2009) Enhancement in leaf photosynthesis and upregulation of Rubisco in the C4 sorghum plant at elevated growth carbon dioxide and temperature occur at early stages of leaf ontogeny. Funct Plant Biol 36:761–769
Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J (2018) Melatonin alleviates high temperature-induced pollen abortion in Solanumlycopersicum. Molecules 23:386
Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104
Rezayian M, Niknam V, Ebrahimzadeh H (2020) Penconazole and calcium ameliorate drought stress in canola by upregulating the antioxidative enzymes. Funct Plant Biol 47:825–839
Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Biol 44:357–384
Rintamäki E, Kettunen R, Aro EM (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. J Biol Chem 271:14870–14875
Rochaix JD (2011) Assembly of the photosynthetic apparatus. Plant Physiol 155:1493–1500
Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88
Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171
Sakamoto W, Zaltsman A, Adam Z, Takahashi Y (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15:2843–2855
Sasi S, Venkatesh J, Daneshi RF, Gururani MA (2018) Photosystem II extrinsic proteins and their putative role in abiotic stress tolerance in higher plants. Plants 7:100
Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98:565–571
Singh-Rawal P, Zsiros O, Bharti S, Garab G, Jajoo A (2011) Mechanism of action of anions on the electron transport chain in thylakoid membranes of higher plants. J Bioenerg Biomembr 43:195–202
Storey R, Ahmad N, Jones RGW (1977) Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants. Oecologia 27:319–332
Sugiura M, Tibiletti T, Takachi I, Hara Y, Kanawaku S, Sellés J, Boussac A (2018) Probing the role of valine 185 of the D1 protein in the photosystem II oxygen evolution. Biochim Biophys Acta Bioenerg 1859:1259–1273
Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19:1347–1361
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60
Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, Badger MR (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993
Theis J, Schroda M (2016) Revisiting the photosystem II repair cycle. Plant Signal Behav 11:e1218587
Tikkanen M, Aro EM (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817:232–238
Tikkanen M, Nurmi M, Kangasjärvi S, Aro EM (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 1777:1432–1437
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60
Wei DD, Zhang W, Wang CC, Meng QW, Li G, Chen TH, Yang XH (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83
Weisz DA, Johnson VM, Niedzwiedzki DM, Shinn MK, Liu H, Klitzke CF, Gross ML, Blankenship RE, Lohman TM, Pakrasi HB (2019) A novel chlorophyll protein complex in the repair cycle of photosystem II. Proc Natl Acad Sci USA 116:21907–21913
Yamamoto Y (2016) Quality control of photosystem II: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids. Front Plant Sci 7:1136
Yang XH, Lu CM (2005) Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol Plant 124:343–352
Yang XH, Liang Z, Lu CM (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 138:2299–2309
Yang XH, Wen XG, Gong HM, Lu QT, Yang ZP, Tang YL, Liang Z, Lu CM (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plant. Planta 225:719–733
Yoshioka-Nishimura M (2016) Close relationships between the PSII repair cycle and thylakoid membrane dynamics. Plant Cell Physiol 57:1115–1122
Zhang TP, Liang JN, Wang MW, Li DX, Liu Y, Chen TH, Yang XH (2019) Genetic engineering of the biosynthesis of glycinebetaine enhances the fruit development and size of tomato. Plant Sci 280:355–366
Zheng J, Bizzozero OA (2009) Traditional reactive carbonyl scavengers do not prevent the carbonylation of brain proteins induced by acute glutathione depletion. Free Radic Res 44:258–266
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This work was supported by the National Natural Sciences Foundation of China (Grant Nos. 31870216, 31470341), the research in Prof. Chen’s laboratory was supported by the Oregon Agricultural Experiment Station.
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XY and TC designed the experiments. DL performed the experiments with the help of MW and TZ Other authors assisted in experiments and discussed the results. DL and XY wrote the manuscript. MB and YL gave positive suggestion about this article. All authors read and approved the manuscript.
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Li, D., Wang, M., Zhang, T. et al. Glycinebetaine mitigated the photoinhibition of photosystem II at high temperature in transgenic tomato plants. Photosynth Res 147, 301–315 (2021). https://doi.org/10.1007/s11120-020-00810-2
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DOI: https://doi.org/10.1007/s11120-020-00810-2