Abstract
Ozone can cause damage to plant tissues. However, little information is available about this global and systematic damage mechanism of grape leaf photosynthetic apparatus. In this study, tandem mass tags (TMT) analysis and physiological responses indicated severe damage to the chloroplasts, with differentially expressed proteins mainly distributed in the chloroplasts. Under ozone stress, the expression of the PSI and PSII structural proteins PsbR, PsaK, PsaA and PSII reactive center protein D1 levels were down-regulated, and the inhibition of D1 protein turnover further aggravated the photodamage of photosystem II (PSII), resulting in a significant decrease in the actual photochemical efficiency of PSII (Y(II)) and actual photochemical efficiency of PSI (Y(I)). The xanthophyll cycle-related protein VDE and ZEP and the NDH subunit of the cyclic electron transport-related protein PGR5-like protein 1A and subcomplex B1 protein were upregulated in response to ozone stress, which was accompanied by a high level of ETRI-ETRII ratio. However, these defense mechanisms are not strong enough. Several dysfunctional antioxidant-related proteins have shown limited ability to scavenge reactive oxygen species, leading to reactive oxygen species burst and eventual photodamage. The system analysis provides new insights into the damage and molecular defense mechanisms of photosynthetic apparatus by ozone.
Similar content being viewed by others
References
Agathokleous E, Kitao M, Qingnan C, Saitanis CJ, Paoletti E, Manning WJ, Watanabe T, Koike T (2018) Effects of ozone (O3) and ethylenediurea (EDU) on the ecological stoichiometry of a willow grown in a free-air exposure system. Environ Pollut 238:663–676
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55(1):373–399
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
Ashmore M (2005) Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 28(8):949–964
Bagard M, Le Thiec D, Delacote E, Hasenfratz-Sauder MP, Banvoy J, Gérard J, Dizengremel P, Jolivet Y (2008) Ozone‐induced changes in photosynthesis and photorespiration of hybrid poplar in relation to the developmental stage of the leaves. Physiol Plant 134(4):559–574
Biswas DK, Xu H, Li YG, Ma BL, Jiang GM (2013) Modification of photosynthesis and growth responses to elevated CO2 by ozone in two cultivars of winter wheat with different years of release. J Exp Bot 64(6):1485–1496
Bussotti F, Strasser RJ, Schaub M (2007) Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. Environ Pollut 147(3):430–437
Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42(6):549–555
Calatayud A, Ramirez JW, Iglesias DJ, Barreno E (2002) Effects of ozone on photosynthetic CO2 exchange, chlorophyll a fluorescence and antioxidant systems in lettuce leaves. Physiol Plant 116(3):308–316
Cao J-L, Wang L, Zeng Q, Liang J, Tang H-Y, Xie Z-B, Liu G, Zhu J-G, Kobayashi K (2009) Characteristics of photosynthesis in wheat cultivars with different sensitivities to ozone under O3-free air concentration enrichment conditions. Acta Agr Sin 35(8):1500–1507
Cao X, Zhu C, Zhong C, Hussain S, Zhu L, Wu L, Jin Q (2018) Mixed-nitrogen nutrition-mediated enhancement of drought tolerance of rice seedlings associated with photosynthesis, hormone balance and carbohydrate partitioning. Plant Growth Regul 84(3):451–465
Che X, Zhang Z, Jin L, Liu M, Li Y, Gao H, Zhao S (2016) Effect of reducing nitric oxide in Rumex K-1 leaves on the photoprotection of photosystem II under high temperature with strong light. J Plant Growth Regul 35(4):1118–1125
Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2017) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81(2):253–264
Degl'Innocenti E, Guidi L, Soldatini GF (2002) Characterisation of the photosynthetic response of tobacco leaves to ozone: CO2 assimilation and chlorophyll fluorescence. J Plant Physiol 159(8):845–853
Dizengremel P, Le Thiec D, Bagard M, Jolivet Y (2008) Ozone risk assessment for plants: central role of metabolism-dependent changes in reducing power. Environ Pollut 156(1):11–15
Du Y-P, Jiang E-S, Wang F-P, Zhang S-Z, Zhai H (2014) Gene expression profiling of rootstock ‘140Ru’and Vitis vinifera L. cv.‘Crimson Seedless’ grape roots infected with grape phylloxera. Plant Growth Regul 73(1):1–8
Elstner EF, Heupel A (1976) Formation of hydrogen peroxide by isolated cell walls from horseradish (Armoracia lapathifolia Gilib.). Planta 130(2):175–180
Eskling M, Arvidsson PO, Åkerlund HE (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100(4):806–816
Feng Z, Uddling J, Tang H, Zhu J, Kobayashi K (2018) Comparison of crop yield sensitivity to ozone between open-top chamber and free‐air experiments. Glob Change Biol 24(6):2231–2238
Geng Q-w, Xing H, Sun Y-j, Hao G-m, Zhai H, Du Y-p (2017) Analysis of the interaction effects of light and O3 on fluorescence properties of ‘Cabernet Sauvignon’grapes based on response surface methodology. Sci Hort 225:599–606
Huang W, Zhang S-B, Hu H (2015) Insusceptibility of oxygen-evolving complex to high light in Betula platyphylla. J Plant Res 128(2):307–315
Huang Y-W, Zhou Z-Q, Yang H-X, Wei C-X, Wan Y-Y, Wang X-J, Bai J-G (2015b) Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity. Biol Plant 59(1):131–138
Iriti M, Faoro F (2008) Oxidative stress, the paradigm of ozone toxicity in plants and animals. Water Air Soil Pollut 187(1–4):285–301
Järvi S, Suorsa M, Tadini L, Ivanauskaite A, Rantala S, Allahverdiyeva Y, Leister D, Aro E-M (2016) Thylakoid-bound FtsH proteins facilitate proper biosynthesis of photosystem I. Plant Physiol 171(2):1333–1343
Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192(2):261–268
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q A redox state and excitation energy fluxes. Photosynth Res 79(2):209
Langebartels C, Wohlgemuth H, Kschieschan S, Grün S, Sandermann H (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40(6–8):567–575
Li P, Calatayud V, Gao F, Uddling J, Feng Z (2016) Differences in ozone sensitivity among woody species are related to leaf morphology and antioxidant levels. Tree Physiol 36(9):1105–1116
Liu Z, Gao J, Gao F, Liu P, Zhao B, Zhang J (2018) Photosynthetic characteristics and chloroplast ultrastructure of summer maize response to different nitrogen supplies. Front Plant Sci 9:576–576
Long S, Naidu S (2002) Effects of oxidants at the biochemical, cell and physiological levels, with particular reference to ozone. Air Pollut Plant Life 2:69–88
Melgar JC, Guidi L, Remorini D, Agati G, Degl’innocenti E, Castelli S, Camilla Baratto M, Faraloni C, Tattini M (2009) Antioxidant defences and oxidative damage in salt-treated olive plants under contrasting sunlight irradiance. Tree Physiol 29(9):1187–1198
Munekage Y, Takeda S, Endo T, Jahns P, Hashimoto T, Shikanai T (2001) Cytochrome b6f mutation specifically affects thermal dissipation of absorbed light energy in Arabidopsis. Plant J 28(3):351–359
Peng Y, Lin W, Wei H, Krebs SL, Arora R (2008) Phylogenetic analysis and seasonal cold acclimation-associated expression of early light-induced protein genes of Rhododendron catawbiense. Physiol Plant 132(1):44–52
Rinnan R, Holopainen T (2004) Ozone effects on the ultrastructure of peatland plants: Sphagnum mosses, Vaccinium oxycoccus, Andromeda polifolia and Eriophorum vaginatum. Ann Bot 94(4):623–634
Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92(3):369–387
Salvatori E, Fusaro L, Mereu S, Bernardini A, Puppi G, Manes F (2013) Different O3 response of sensitive and resistant snap bean genotypes (Phaseolus vulgaris L.): the key role of growth stage, stomatal conductance, and PSI activity. Environ Exp Bot 87:79–91
Schaub M, Calatayud V (2013) Assessment of visible foliar injury induced by ozone. Elsevier, Amsterdam, pp 205–221
Sgarbi E, Baroni Fornasiero R, Paulino Lins A, Medeghini Bonatti P (2003) Phenol metabolism is differentially affected by ozone in two cell lines from grape (Vitis vinifera L.) leaf. Plant Sci 165(5):951–957
Solomon S, Qin D, Manning M, Averyt K, Marquis M (2007) Climate change 2007-the physical science basis: working group I contribution to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge
Strasser B, Strasser R (1995) Measuring fast fluorescence transients to address environmental questions: the JIP test, P. Mathis (Ed.), Photosynthesis: from light to biosphere, vol. V. In: Proceedings of the Xth international photosynthesis congress. Montpellier, France, Kluwer Academic Publishers, Dordrecht
Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) 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. Biochim Biophys Acta (BBA) 1797(6–7):1313–1326
Sun Y, Gao Y, Wang H, Yang X, Zhai H, Du Y (2018) Stimulation of cyclic electron flow around PSI as a response to the combined stress of high light and high temperature in grape leaves. Funct Plant Biol 45(10):1038–1045
Sun Y, Geng Q, Du Y, Yang X, Zhai H (2017) Induction of cyclic electron flow around photosystem I during heat stress in grape leaves. Plant Sci 256:65–71
Sun Y, Liu X, Zhai H, Gao H, Yao Y, Du Y (2016) Responses of photosystem II photochemistry and the alternative oxidase pathway to heat stress in grape leaves. Acta Physiol Plant 38(10):232
Tiwari S, Agrawal M (2018) Ozone concentrations in troposphere: historical and current perspectives. Tropospheric ozone and its impacts on crop plants. Springer, New York, pp 1–29
Tran TA, Vassileva V, Petrov P, Popova LP (2013) Cadmium-induced structural disturbances in Pisum sativum leaves are alleviated by nitric oxide. Turk J Bot 37(4):698–707
Valletta A, Salvatori E, Rita Santamaria A, Nicoletti M, Toniolo C, Caboni E, Bernardini A, Pasqua G, Manes F (2016) Ecophysiological and phytochemical response to ozone of wine grape cultivars of Vitis vinifera L. Nat Prod Res 30(22):2514–2522
Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye J-Y, Mi H (2006) Chloroplastic NAD (P) H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol 141(2):465–474
Wei S, Wang X, Jiang D, Dong S (2018) Physiological and proteome studies of maize (Zea mays L.) in response to leaf removal under high plant density. BMC Plant Biol 18(1):378
Wilhelm C, Selmar D (2011) Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis. J Plant Physiol 168(2):79–87
Xing X, Liu Y, Kong X, Liu Y, Li D (2011) Overexpression of a maize dehydrin gene, ZmDHN2b, in tobacco enhances tolerance to low temperature. Plant Growth Regul 65(1):109–118
Xu L, Yue Q, Bian Fe, Sun H, Zhai H, Yao Y (2017) Melatonin enhances phenolics accumulation partially via ethylene signaling and resulted in high antioxidant capacity in grape berries. Front Plant Sci 8:1426
Xu X, Guo K, Liang W, Chen Q, Shi J, Shen B (2018) Quantitative proteomics analysis of proteins involved in leaf senescence of rice (Oryza sativa L.). Plant Growth Regul 84(2):341–349
Yamamoto H, Kato H, Shinzaki Y, Horiguchi S, Shikanai T, Hase T, Endo T, Nishioka M, Makino A, Tomizawa K-i, Miyake C (2006) Ferredoxin limits cyclic electron flow around PSI (CEF-PSI) in higher plants-stimulation of CEF-PSI enhances non-photochemical quenching of Chl fluorescence in transplastomic tobacco. Plant Cell Physiol 47(10):1355–1371
Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (2011) Cyclic electron flow around photosystem I via chloroplast NAD (P) H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68(6):966–976
Zhang W, Feng Z, Wang X, Niu J (2012) Responses of native broadleaved woody species to elevated ozone in subtropical China. Environ Pollut 163:149–157
Zheng YH, Li X, Li YG, Miao BH, Xu H, Simmons M, Yang XH (2012) Contrasting responses of salinity-stressed salt-tolerant and intolerant winter wheat (Triticum aestivum L.) cultivars to ozone pollution. Plant Physiol Biochem 52:169–178
Zheng YH, Li YG, Xia WR, Xu H, Su BY, Jiang GM, Ning TY (2011) Responses of gas exchange, cellular membrane integrity, and antioxidant enzymes activities of salinity-stressed winter wheat to ozone pollution. Photosynthetica 49(3):389
Zhuang M, Lam SK, Li Y, Chen S (2017) Elevated tropospheric ozone affects the concentration and allocation of mineral nutrients of two bamboo species. Sci Total Environ 577:231–235
Acknowledgements
This research was supported by the National Key Research and Development Program of China (2019YFD1000101), National Natural Sciences Foundation of China in 2016 (31572084), China agricultural research system (CARS-29), and Program for Changjiang Scholars and Innovative Research Team in University (IRT15R42).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10725_2020_593_MOESM2_ESM.tif
Supplementary material 2 (TIF 411.1 kb). Figure S1. Quality detection of mass spectrometry data. (A) Protein sequences coverage of different molecular weight. (B) Error distribution of spectra match quality of grape leaves. (C) Number of peptide length distributed in our mass spectrometry data of grape leaves
Rights and permissions
About this article
Cite this article
Chen, Z., Gao, Z., Sun, Y. et al. Analyzing the grape leaf proteome and photosynthetic process provides insights into the injury mechanisms of ozone stress. Plant Growth Regul 91, 143–155 (2020). https://doi.org/10.1007/s10725-020-00593-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-020-00593-5