Abstract
The xanthophyll cycle plays a pivotal role in protecting plants and algae against photodamage. Although the resistance of the violaxanthin de-epoxidase enzyme (VDE) to high light stress in the xanthophyll cycle has been extensively studied, there is limited knowledge about VDE-related (VDR) proteins, which exhibit a close homologous relationship with VDEs. In this study, we preliminary investigated VDR protein, focusing on basic bioinformatics, spatiotemporal gene expression patterns, and high light stress treatment. VDR exhibited a significant homology with VDE, and the CsVDR protein was localized in the chloroplasts. CsVDR was expressed in all tissues of Arabidopsis and cucumber, with the highest expression level observed in mature leaves cultivated for 20 days in cucumber. Interestingly, both CsVDR and AtVDR were identified as high light response genes. Under high light stress, the non-photochemical quenching and Fv/Fm exhibited a decrease in both the Atvdr mutants and TRSV::CsVDR lines compared to the WT. Additionally, the de-epoxidation ratio (A + Z)/(A + Z + V) of the Atvdr mutants was significantly reduced. This suggested that the xanthophyll cycle in Atvdr mutants and TRSV::CsVDR lines were less effective and more susceptible to photoinhibition of PSII under high light stress. Our findings provide compelling evidence for the involvement of VDR proteins in regulating plant response to high light, thereby offering a theoretical basis for further investigation into plant photoprotective pathways.
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References
Adams BD (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochem Biophys Acta 1020:1–24
Adams BD, Adams WW (1991) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1(1):21–26
Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21(7):2036–2044
Bartholomew ES, Xu S, Zhang Y, Yin S, Feng Z, Chen S, Sun L, Yang S, Wang Y, Liu P, Ren H, Liu X (2022) A chitinase CsChi23 promoter polymorphism underlies cucumber resistance against Fusarium oxysporum f. sp. Cucumerinum. New Phytol 236(4):1471–1486
Bassi B, Dall’Olsto L (2021) Dissipation of light energy absorbed in excess: the molecular mechanisms. Ann Rev Plant Biol 72:47–76. https://doi.org/10.1146/annurev-arplant-071720-015522
Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci USA 93(13):6320–6325
Bugos RC, Hieber AD, Yamamoto HY (1998) Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Chem 273(25):15321–15324
Cazzaniga S, Dall’ Osto L, Kong SG, Wada M, Bassi R (2013) Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. Plant J: Cell Mol Bio 76(4):568–579
Chang SH, Bugos RC, Sun WH, Yamamoto HY (2000) Antisense suppression of violaxanthin de-epoxidase in tobacco does not affect plant performance in controlled growth conditions. Photosynth Res 64(1):95–103
Chen L, Yan Z, Xia Z, Cheng Y, Jiao Z, Sun B, Zhou T, Fan Z (2017) A violaxanthin deepoxidase interacts with a viral suppressor of RNA silencing to inhibit virus amplification. Plant Physiol 175(4):1774–1794
Coesel S, Oborník M, Varela J, Falciatore A, Bowler C (2008) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS ONE 3(8):e2896
Dautermann O, Lyska D, Andersen-Ranberg J, Becker M, Fröhlich-Nowoisky J, Gartmann H, Krämer LC, Mayr K, Pieper D, Rij LM, Wipf HM, Niyogi KK, Lohr M (2020) An algal enzyme required for biosynthesis of the most abundant marine carotenoids. Sci Adv 6(10):eaaw9183
De Souza AP, Burgess SJ, Doran L, Hansen J, Manukyan L, Maryn N, Gotarkar D, Leonelli L, Niyogi KK, Long SP (2022) Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science 377(6608):851–854
Emanuelsson A, Eskling M, Akerlund HE (2003) Chemical and mutational modification of histidines in violaxanthin de-epoxidase from spinacia oleracea. Physiol Plant 119(97):104
Fang L, Wei XY, Liu LZ, Zhou LX, Tian YP, Geng C, Li XD (2021) A tobacco ringspot virus-based vector system for gene and microRNA function studies in cucurbits. Plant Physiol 186(2):853–864
Flower DR, North AC, Attwood TK (1993) Structure and sequence relationships in the lipocalins and related proteins. Protein Sci 2(5):753–761
Gao S, Han H, Feng HL, Zhao SJ, Wei Q (2010) Overexpression and suppression of violaxanthin de-epoxidase affects the sensitivity of photosystem photoinhibition to high light and chilling stress in transgenic tobacco. J Integr Plant Biol 52(3):332–339
Girolomoni L, Bellamoli F, de la Cruz VG, Perozeni F, D’Andrea C, Cerullo G, Cazzaniga S, Ballottari M (2020) Evolutionary divergence of photoprotection in the green algal lineage: a plant-like violaxanthin de-epoxidase enzyme activates the xanthophyll cycle in the green alga Chlorella vulgaris modulating photoprotection. New Phytol 228(1):136–150
Guan C, Ji J, Zhang X, Li X, Jin C, Guan W, Wang G (2014) Positive feedback regulation of a Lycium chinense-derived VDE gene by drought-induced endogenous ABA, and over-expression of this VDE gene improve drought-induced photo-damage in Arabidopsis. J Plant Physiol 175:26–36
Hager A (1969) Light dependent decrease of the pH-value in a chloroplast compartment causing the enzymatic interconversion of violaxanthin to zeaxanthin; relations to photophosphorylation. Planta 89(3):224–243
Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167(3):176–183
Havaux M, Bonfils JP, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124(1):273–284
He WJ, Ya K, Zhang Y, Bian LX, Mei HM, Han GX (2021) Contrasting photosynthesis, photoinhibition and oxidative damage in honeysuckle (Lonicera japonica Thunb.) under isosmotic salt and drought stresses. Enviro Exp Bot. 182:104313
Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochem Biophys Acta 1482(1–2):84–91
Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts IV. Resolution of non-photochemical quenching. BBA-Bioenerg 932(1):107–115
Huang H, Wang Z, Cheng J, Zhao W, Li X, Wang H, Zhang Z, Sui X (2013) An efficient cucumber (Cucumis sativus L.) protoplast isolation and transient expression system. Sci Hortic 150:206–212
Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochem Biophys Acta 1787(1):3–14
Jin H, Liu B, Luo L, Feng D, Wang P, Liu J, Da Q, He Y, Qi K, Wang J, Wang HB (2014) Hypersensitive to high light1 interacts with low quantum yield of photosystem II1 and functions in protection of photosystem II from photodamage in Arabidopsis. Plant Cell 26(3):1213–1229
Li X, Zhao W, Sun X, Huang H, Kong L, Niu D, Sui X, Zhang Z (2013) Molecular cloning and characterization of violaxanthin de-epoxidase (CsVDE) in cucumber. PLoS ONE 8(5):e64383
Lin W, Yu Z, Luo Y, He W, Yan G, Peng C (2022) Photoprotection differences between dominant tree species at mid- and late-successional stages in subtropical forests in different seasonal environments. Int J Mol Sci 23(10):5417
Liu S, Liu C, Wang X, Chen H (2021) Seed-specific activity of the Arabidopsis β-glucosidase 19 promoter in transgenic Arabidopsis and tobacco. Plant Cell Rep 40(1):213–221
Müller-Moulé P, Conklin PL, Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128(3):970–977
Murchie EK, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10(7):1121–1134
Payton P, Webb R, Kornyeyev D, Allen R, Holaday AS (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J Exp Bot 52(365):2345–2354
Plazapla JIG, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34(9):759–773
Retkute R, Smith-Unna SE, Smith RW, Burgess AJ, Jensen OE, Johnson GN, Preston SP, Murchie EH (2015) Exploiting heterogeneous environments: does photosynthetic acclimation optimize carbon gain in fluctuating light? J Exp Bot 66(9):2437–2447
Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916
Saga G, Giorgetti A, Fufezan C, Giacometti GM, Bassi R, Morosinotto T (2010) Mutation analysis of violaxanthin de-epoxidase identifies substrate-binding sites and residues involved in catalysis. J Biol Chem 285(31):23763–23770
Sun LN, Wang F, Wang JW, Sun LJ, Gao WR, Song XS (2019) Overexpression of the ChVDE gene, encoding a violaxanthin de-epoxidase, improves tolerance to drought and salt stress in transgenic Arabidopsis. 3 Biotech 9(5):197
Wang X, Ren P, Ji L, Zhu B, Xie G (2021) OsVDE, a xanthophyll cycle key enzyme, mediates abscisic acid biosynthesis and negatively regulates salinity tolerance in rice. Planta. https://doi.org/10.1007/s00425-021-03802-1
Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327
Yan K, Wu C, Zhang L, Chen X (2015) Contrasting photosynthesis and photoinhibition in tetraploid and its autodiploid honeysuckle (Lonicera japonica Thunb.) under salt stress. Front Plant Sci 6:227
Acknowledgements
We thank Prof. Zhenxian Zhang (College of Horticulture, China Agricultural University) for providing the initial idea for this paper
Funding
This work was supported by the National Natural Science Foundation of China (grant nos. 31801850), the National Key Research and Development Program of China (2019YFD1000300), the 111 Project (B17043), and the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects (CEFF-PXM2019_014207_000032). Beijing Innovation Consortium of Agriculture Research System (BAIC12-2024, BAIC01-2024). China Agriculture Research System (CAS-23).
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Zhenxian Zhang and Xin Li contributed to the study conception. Lihong Gao, Yongqiang Tian, and Si Ma participated in the experimental design. Jing Zhang and Shi Zhang performed the experiment. Weike Sun, Yichao Huang and Syed Aizaz Ali Shah collected samples and statistical data. Hongyu Huang provided the necessary resources for research completion. The first draft of the manuscript was written by Shi Zhang, Xin Li, and Jingwei Wei reviewed the draft. All authors contributed to the article and approved the submission.
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Supplementary file1 (XLSX 27 kb)—The sequence information of proteins used for the phylogenetic 602 development analysis within algae and terrestrial plants.
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Wei, J., Huang, H., Zhang, S. et al. Functions of violaxanthin de-epoxidase-related (VDR) in the photoprotective response to high-light stress. Plant Growth Regul (2024). https://doi.org/10.1007/s10725-024-01158-6
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DOI: https://doi.org/10.1007/s10725-024-01158-6