Abstract
Hydrogen gas (H2) has recently been recognized as an important plant bio-regulator, inducing tolerance to several abiotic stresses. However, any role for H2 in amelioration of high-temperature-induced stress remains largely unknown. We investigated the mechanism of hydrogen-rich water (HRW)-mediated enhancement of heat-tolerance in cucumber seedlings exposed to high-temperature stress. The 3 weeks seedlings were pretreated with 50 or 100% HRW for 7 days, the effects on photosynthesis, chlorophyll content, chlorophyll fluorescence parameters, electrolyte leakage, lipid peroxidation, and antioxidant activity were examined when cucumber seedlings subjected for 3 days to heat stress treatment. With respect to samples treat with high temperature stress alone, HRW pretreatment remarkably alleviated stress-induced effects on the above parameters. Furthermore, after 3 days of treatment, HRW pretreatment also significantly increased the activities of antioxidative enzymes, promoted high-level accumulation of osmoprotectants, and upregulated HSP70 expression in cucumber leaves. All of these data suggest that pretreatment with exogenous HRW partially alleviated the detrimental effects of high-temperature stress on the growth of cucumber seedlings by improving the photosynthetic capacity, increasing the antioxidant response, and promoting the accumulation of HSP70 and osmolytes. Therefore, HRW pretreatment may improve cucumber seedlings heat-tolerance.
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Abbreviations
- APX:
-
Ascorbate peroxidase
- AsA:
-
Ascorbic acid
- CAT:
-
Catalase
- Chl:
-
Chlorophyll
- Ci:
-
Intercellular CO2 concentration
- D:
-
The fraction of absorbed light energy dissipated through non-photochemical quenching
- E:
-
The fraction of excess absorbed light energy
- ETR:
-
Electron transport rate
- Fv/Fm:
-
Maximal quantum efficiency of Photosystem II
- Fv′/Fm′:
-
The excitation capture efficiency of open centers
- Gm:
-
Mesophyll conductance
- Gs:
-
Stomatal conductance
- GSH:
-
Glutathione
- H2O2 :
-
Hydrogen peroxide
- HRW:
-
Hydrogen-rich water
- HSPs:
-
Heat shock proteins
- HT:
-
High temperature
- MDA:
-
Malondialdehyde
- NBT:
-
Nitroblue tetrazolium
- P:
-
The fraction of absorbed light energy utilized in Photosystem II photochemistry
- Pn:
-
Net photosynthetic rate
- POD:
-
Peroxidase
- PPFD:
-
Photosynthetic photon flux density
- PSII:
-
Photosystem II
- qP:
-
Photochemical quenching
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- Tr:
-
Transpiration rate
- WUE:
-
Water use efficiency
- ΦPSII:
-
Quantum efficiency of Photosystem II
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Anastasis C, Panagiota F, George AM, Vasileios F (2013) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14(1):42
Andre CM, Yvan L, Daniele E (2010) Dietary antioxidants and oxidative stress from a human and plant perspective: a review. Curr Nutr Food Sci 6:2–12
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216
Ashraf M, Hafeez M (2004) Thermotolerance of pearl millet and maize at early growth stages: growth and nutrient relations. Biol Plant 48(1):81–86
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190
Asthir B, Koundal A, Bains NS (2012) Putrescine modulates antioxidant defense response in wheat under high temperature stress. Biol Plant 56(4):757–761
Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152(3):1471–1483
Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2012) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32(1):216–232
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207
Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15(6):330–336
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72(1–2):248–254
Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44(267):1627–1629
Chen M, Cui WT, Zhu KK, Xie YJ, Zhang CH, Shen WB (2014) Hydrogen-rich water alleviates aluminum-induced inhibition of root elongation in alfalfa via decreasing nitric oxide production. J Hazard Mat 267:40–47
Christensen HT, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11(6):1187–1194
Cui WT, Gao CY, Fang P, Lin GQ, Shen WB (2013) Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J Hazard Mat 260:715–724
Cui WT, Fang P, Zhu K (2014) Hydrogen-rich water confers plant tolerance to mercury toxicity in alfalfa seedlings. Ecotoxicol Environ Saf 105(105):103–111
Demmig-Adams B, Iii WWA, Barker DH (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98(2):253–264
Djanaguiraman M, Sheeba JA, Devi DD, Bangarusamy U (2009) Cotton leaf senescence can be delayed by nitrophenolate spray through enhanced antioxidant defense system. J Agron Crop Sci 195(3):213–224
Dong Z, Wu L, Kettlewell B, Caldwell CD, Layzell DB (2003) Hydrogen fertilization of soils-is this a benefit of legumes in rotation. Plant Cell Environ 26:1875–1879
Garbero M, Pedranzani H, Zirulnik F, Molina A, Pérez-Chaca MV, Vigliocco A, Abdala G (2011) Short-term cold stress in two cultivars of Digitaria eriantha: effects on stress-related hormones and antioxidant defense system. Acta Physiol Plant 33:497–507
Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59(2):309–314
Golding L, Dong Z (2010) Hydrogen production by nitrogenase as a potential crop rotation benefit. Environ Chem Lett 8(2):101–121
González L, González-Vilar M (2003) Determination of relative water content and electrolytic leakage. In: Roger MJR (ed) Handbook of plant ecophysiology techniques. Springer, Dordrecht, pp 207–212
Greer DH, Weedon MM (2012) Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate. Plant Cell Environ 35(6):1050–1064
Guo FX, Zhang MX, Chen Y, Zhang WH, Xu SJ, Wang JH, An LZ (2006) Relation of several antioxidant enzymes to rapid freezing resistance in suspension cultured cells from alpine Chorispora bungeana. Cryobiology 52(2):241–250
Hagemann M, Fernie AR, Espie GS, Kern R, Eisenhut M, Reumann S, Bauwe H, Weber APM (2013) Evolution of the biochemistry of the photorespiratory C2 cycle. Plant Biol (Stuttg) 15:639–647
Hu H, Li P, Wang YN, Gu RX (2014) Hydrogen-rich water delays postharvest ripening andsenescence of kiwifruit. Food Chem 156(11):100–109
Huang CS, Kawamura T, Toyoda Y, Nakao A (2010) Recent advances in hydrogen research as a therapeutic medical gas. Free Radic Res 44(9):971–982
Huerta C, Freire M, Cardemil L (2013) Expression of hsp70, hsp100 and ubiquitin in Aloe barbadensis Miller under direct heat stress and under temperature acclimation conditions. Plant Cell Rep 32:293–307
Jin QJ, Zhu KK, Cui WT, Xie YJ, Han B, Shen WB (2013) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ 36:956–969
Jones MM, Turner NC (1978) Osmotic adjustment in leaves of sorghum in response to water deficits. Plant Physiol 61(1):122–126
Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiol 60:606–608
Kumar S, Kaur R, Kaur N, Bhandhari K, Kaushal N, Gupta K, Bains TS, Nayyar H (2011) Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol Plant 3:2091–2101
Liu CC, Liu YG, Guo K, Fan D, Li G, Zheng YR, Yu LF, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183
Liu ZX, Bie ZL, Huang Y, Zhen A, Lei B, Zhang HY (2012) Grafting onto Cucurbita moschata rootstock alleviates salt stress in cucumber plants by delaying photoinhibition. Photosynthetica 50(1):152–160
Lu CM, Zhang JH (2000) Heat-induced multiple effects on PS II in wheat plants. J Plant Physiol 156:259–265
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767(6):414–421
Neves JPC, Ferreira LFP, Vaz MM, Gazarini LC (2008) Gas exchange in the salt marsh species Atriplex portulacoides L. and Limoniastrum monopetalum L. in Southern Portugal. Acta Physiol Plant 30(1):91–97
Nigro A, Mauro L, Giordano F, Panza S, Iannacone R, Liuzzi GM, Aquila S, De A F, Cellini F, Indiveri C, Panno ML (2016) Recombinant Arabidopsis HSP70 sustains cell survival and metastatic potential of breast cancer cells. Mol Cancer Ther 15(5):1063–1073
Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S (2007) Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13:688–694
Öquist G, Chow WS (1992) On the relationship between the quantum yield of Photosystem II electron transport, as determined by chlorophyll fluorescence and the quantum yield of CO2 − dependent O2 evolution. Photosynth Res 33(1):51–62
Renwick GM, Giumarro C, Siegel SM (1964) Hydrogen metabolism in higher plants. Plant Physiol 39(3):303–306
Ristic Z, Williams G, Yang G, Martin B, Fullerton S (1996) Dehydration, damage to cellular membranes, and heat-shock proteins in maize hybrids from different climates. J Plant Physiol 149(3):424–432
Sanadze GA (1961) Absorption of molecular hydrogen by green leaves in light. Fiziol Rast 8:555–559
Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52(8):712–722
Strasser RJ, Srivastava A, Tsmilli-Michael M (2004) Analysis of the chlorophyll fluorescence transient, vol 19. Kluwer Academic Publishers, Berlin, pp 321–362
Su NN, Wu Q, Liu YY, Cai JT, Shen WB, Xia K (2014) Hydrogen-rich water reestablishes ROS homeostasis but exerts differential effects on anthocyanin synthesisin two varieties of radish sprouts under UV-A irradiation. J Agric Food Chem 62(27):6454
Suleman P, Redha A, Afzal M, Al-Hasan R (2012) Temperature-induced changes of malondialdehyde, heat-shock proteins in relation to chlorophyll fluorescence and photosynthesis in Conocarpus lancifolius. Acta Physiol Plant 28:1–9
Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25(3):147–150
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous polyammines. Plant Sci 151:59–66
Wen XG, Gong HM, Lu CM (2005) Heat stress induces a reversible inhibition of electron transport at the acceptor side of photosystem II in a cyanobacterium Spirulina platensis. Plant Sci 168(6):1471–1476
White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59(1):63–72
Wu XX, Yao XF, Chen JL, Zhu ZW, Zhang H, Zha DS (2014) Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol Plant 36:251–261
Xie YJ, Mao Y, Lai DW, Zhang W, Shen WB (2012) H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS One 7(11):e49800
Xie YJ, Mao W, Zhang W, Wang QY, Shen WB (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiol 165(2):759–773
Xu S, Zhu SS, Jiang YL, Wang N, Wang R, Shen WB, Yang J (2013) Hydrogen-rich water alleviates salt stress in rice during seed germination. Plant Soil 370:47–57
Zeng JQ, Zhang MY, Sun XJ (2013) Molecular hydrogen is involved in phytohormone signaling and stress responses in plants. PLOS One 8(8):e71038
Zhang XN, Zhao XQ, Wang ZQ (2015) Protective effects of hydrogen-rich water on the photosynthetic apparatus of maize seedlings (Zea mays L.) as a result of an increase in antioxidant enzyme activities under high light stress. Plant Growth Regul 77(1):43–56
Zhu JJ, Zhang JL, Liu HC, Cao KF (2009) Photosynthesis, non-photochemical pathways and activities of antioxidant enzymes in a resilient evergreen oak under different climatic conditions from a valley-savanna in Southwest China. Physiol Plant 135:62–72
Zhu XC, Song FB, Liu SQ, Liu TD (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346:189–199
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This project was supported by the National Natural Science Foundation of China (J1210056).
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Chen, Q., Zhao, X., Lei, D. et al. Hydrogen-rich water pretreatment alters photosynthetic gas exchange, chlorophyll fluorescence, and antioxidant activities in heat-stressed cucumber leaves. Plant Growth Regul 83, 69–82 (2017). https://doi.org/10.1007/s10725-017-0284-1
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DOI: https://doi.org/10.1007/s10725-017-0284-1