Abstract
Hydrogen (H2), an endogenous gaseous molecule, plays a significant role in plant development and stress responses. Here, we investigated the effects of hydrogen-rich water (HRW) pretreatment on 64 parameters, including germination rate, growth indexes, sugar mobilization, reactive oxygen homeostasis, enzymatic and non-enzymatic antioxidants defense system under drought of barley (Hordeum vulgare L.). The results showed that exogenous H2 supplies differentially attenuated the damage of germination and seedling establishment by drought. Compared to samples treated with drought stress alone, HRW pretreatment promoted germination rate and seedling morphological parameters (length and number of root, length of shoot and coleoptile). Further research exhibited HRW could elevate reducing sugar content, α-amylase activity, and β-amylase activity in the seed, significantly decreased the membrane injury index, superoxide radical (O2−) level and hydrogen peroxide (H2O2) level, increased the activities of ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), and glutathione reductase (GR), both in root and shoot. What is more, exogenous H2 also promoted ascorbate (AsA) content and glutathione (GSH) content, reduced dehydroascorbic acid (DHA) content and glutathione disulfide (GSSG) content to different degrees, which led to AsA/DHA ratio and GSH/GSSG ratio increase. The above results combined with correlation analysis and principal component analysis suggested that HRW (especially 25% HRW) pretreatment could mitigate drought-induced damage enabled by activating sugar metabolism through up-regulating amylase activity, reestablishing redox balance through regulating the ascorbate-glutathione (ASA-GSH) cycle.
Similar content being viewed by others
Data Availability
The data will be made available on reasonable request.
Abbreviations
- O2 − :
-
Superoxide radical
- APX:
-
Ascorbate peroxidase
- AsA:
-
Ascorbate
- ASA-GSH:
-
Ascorbate-glutathione
- DHA:
-
Dehydroascorbic acid
- DHAR:
-
Dehydroascorbate reductase
- GIR:
-
Growth inhibition rate of root
- GIS:
-
Growth inhibition rate of shoot
- GR:
-
Glutathione reductase
- GSH:
-
Glutathione
- GSSG:
-
Glutathione disulfide
- H2 :
-
Hydrogen
- H2O2 :
-
Hydrogen peroxide
- HRW:
-
Hydrogen-rich water
- MDHA:
-
Monodehydroascorbate
- MDHAR:
-
Monodehydroascorbate reductase
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
References
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24(12):1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Bai Y, Xiao S, Zhang Z, Zhang Y, Sun H, Zhang K, Wang X, Bai Z, Li C, Liu L (2020) Melatonin improves the germination rate of cotton seeds under drought stress by opening pores in the seed coat. PeerJ 8:e9450. https://doi.org/10.7717/peerj.9450
Betts NS, Wilkinson LG, Khor SF, Shirley NJ, Lok F, Skadhauge B, Burton RA, Fincher GB, Collins HM (2017) Morphology, carbohydrate distribution, gene expression, and enzymatic activities related to cell wall hydrolysis in four barley varieties during simulated malting. Front Plant Sci 8:1872. https://doi.org/10.3389/fpls.2017.01872
Chen Q, Zhao X, Lei D, Hu S, Shen Z, Shen W, Xu X (2017) Hydrogen-rich water pretreatment alters photosynthetic gas exchange, chlorophyll fluorescence, and antioxidant activities in heat-stressed cucumber leaves. Plant Growth Regul 83(1):69–82. https://doi.org/10.1007/s10725-017-0284-1
Cui W, Gao C, Fang P, Lin G, Shen W (2013) Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J Hazard Mater 260:715–724. https://doi.org/10.1016/j.jhazmat.2013.06.032
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147. https://doi.org/10.3389/fpls.2017.01147
FAOSTAT (2019) Food and Agriculture Organization of the United Nations Statistics Division. FAO, Rome. Available from http://www.fao.org/faostat/en/#data/QCL
Felix K, Su J, Lu R, Zhao G, Cui W, Wang R, Mu H, Cui J, Shen W (2019) Hydrogen-induced tolerance against osmotic stress in alfalfa seedlings involves ABA signaling. Plant Soil 445(1–2):409–423. https://doi.org/10.1007/s11104-019-04328-y
Flint HL, Boyce BR, Beattie DJ (1967) Index of injury-A useful expression of freezing injury to plant tissues as determined by the electrolytic method. Can J Plant Sci 47(2):229–230. https://doi.org/10.4141/cjps67-043
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18. https://doi.org/10.1104/pp.110.167569
Foyer CH (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot 154:134–142. https://doi.org/10.1016/j.envexpbot.2018.05.003
Fröhlich M, Kutschera U (1995) Changes in soluble sugars and proteins during development of rye coleoptiles. J Plant Physiol 146(1–2):121–125. https://doi.org/10.1016/s0176-1617(11)81977-2
Garapati P, Xue GP, Munné-Bosch S, Balazadeh S (2015) Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol 168(3):1122–1139. https://doi.org/10.1104/pp.15.00567
Gibert A, Gray EF, Westoby M, Wright IJ, Falster DS (2016) On the link between functional traits and growth rate: meta-analysis shows effects change with plant size, as predicted. J Ecol 104(5):1488–1503. https://doi.org/10.1111/1365-2745.12594
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Goharrizi KJ, Baghizadeh A, Kalantar M, Fatehi F (2019) Combined effects of salinity and drought on physiological and biochemical characteristics of pistachio rootstocks. Sci Hortic 261:108970. https://doi.org/10.1016/j.scienta.2019.108970
Goharrizi KJ, Baghizadeh A, Kalantar M, Fatehi F (2020a) Assessment of changes in some biochemical traits and proteomic profile of UCB-1 pistachio rootstock leaf under salinity stress. J Plant Growth Regul 39(2):608–630. https://doi.org/10.1007/s00344-019-10004-3
Goharrizi KJ, Moosavi SS, Amirmahani F, Salehi F, Nazari M (2020b) Assessment of changes in growth traits, oxidative stress parameters, and enzymatic and non-enzymatic antioxidant defense mechanisms in Lepidium draba plant under osmotic stress induced by polyethylene glycol. Protoplasma 257(2):459–473. https://doi.org/10.1007/s00709-019-01457-0
Goharrizi KJ, Riahi-Madvar A, Rezaee F, Pakzad R, Bonyad FJ, Ahsaei MG (2020c) Effect of salinity stress on enzymes’ activity, ions concentration, oxidative stress parameters, biochemical traits, content of sulforaphane, and CYP79F1 gene expression level in Lepidium draba plant. J Plant Growth Regul 39(3):1075–1094. https://doi.org/10.1007/s00344-019-10047-6
Goharrizi KJ, Meru G, Kermani SG, Heidarinezhad A, Salehi F (2021) Short-term cold stress affects physiological and biochemical traits of pistachio rootstocks. S Afr J Bot 141:90–98. https://doi.org/10.1016/j.sajb.2021.04.029
Guan Q, Ding XW, Jiang R, Ouyang PL, Cui J, Feng L, Yang L, Song LH (2019) Effects of hydrogen-rich water on the nutrient composition and antioxidative characteristics of sprouted black barley. Food Chem 299:125095. https://doi.org/10.1016/j.foodchem.2019.125095
Gupta A, Rico-Medina A, Caño -Delgado AI, (2020) The physiology of plant responses to drought. Science 368(6488):266–269. https://doi.org/10.1126/science.aaz7614
Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, AL Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8(9):384. https://doi.org/10.3390/antiox8090384
Hellal FA, El-Shabrawi HM, Abd El-Hady M, Khatab IA, El-Sayed SAA, Abdelly C (2018) Influence of PEG induced drought stress on molecular and biochemical constituents and seedling growth of Egyptian barley cultivars. J Genet Eng Biotechnol 16(1):203–212. https://doi.org/10.1016/j.jgeb.2017.10.009
Huang C, Qin N, Sun L, Yu M, Hu W, Qi Z (2018) Selenium improves physiological parameters and alleviates oxidative stress in strawberry seedlings under low-temperature stress. Int J Mol Sci 19(7):1913. https://doi.org/10.3390/ijms19071913
Hussaan M, Tanwir K, Abbas S, Javed MT, Iqbal N (2021) Zinc-lysine (Zn-Lys) decipher cadmium tolerance by improved antioxidants, nutrient acquisition, and diminished Cd retention in two contrasting wheat cultivars. J Plant Growth Regul (online). https://doi.org/10.1007/s00344-021-10528-7
Kiarash JG, Wilde HD, Amirmahani F, Moemeni MM, Zaboli M, Nazari M, Moosavi SS, Jamalvandi M (2018) Selection and validation of reference genes for normalization of qRT-PCR gene expression in wheat (Triticum durum L.) under drought and salt stresses. J Genet Genomics 97(5):1433–1444. https://doi.org/10.1007/s12041-018-1042-5
Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts-the effect of hydrogen peroxide and of Paraquat. Biochem J 210(3):899–903. https://doi.org/10.1042/bj2100899
Li BH, Sun L, Huang JY, Göschl C, Shi WM, Chory J, Busch W (2019) GSNOR provides plant tolerance to iron toxicity via preventing iron-dependent nitrosative and oxidative cytotoxicity. Nat Commun 10:3896. https://doi.org/10.1038/s41467-019-11892-5
Ma L, Kong L, Gui R, Yang X, Zhang J, Gong Q, Qin D, Zhuang M, Ashraf U, Mo Z (2021) Application of hydrogen-rich water modulates physio-biochemical functions and early growth of fragrant rice under Cd and Pb stress. Environ Sci Pollut Res 28(41):58558–58569. https://doi.org/10.1007/s11356-021-14747-z
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nazari M, Goharrizi KJ, Moosavi SS, Maleki M (2019) Expression changes in the TaNAC2 and TaNAC69-1 transcription factors in drought stress tolerant and susceptible accessions of Triticum boeoticum. Plant Genet 17(6):471–479. https://doi.org/10.1017/S1479262119000303
Nazari M, Moosavi SS, Maleki M, Goharrizi KJ (2020) Chloroplastic acyl carrier protein synthase I and chloroplastic 20 kDa chaperonin proteins are involved in wheat (Triticum aestivum) in response to moisture stress. J Plant Interact 15(1):180–187. https://doi.org/10.1080/17429145.2020.1758812
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(6):688–694. https://doi.org/10.1038/nm1577
Qiu CW, Liu L, Feng X, Hao PF, He X, Cao F, Wu F (2020) Genome-wide identification and characterization of drought stress responsive microRNAs in Tibetan wild barley. Int J Mol Sci 21(8):2795. https://doi.org/10.3390/ijms21082795
Rico D, Peñas E, García MD, Martínez-Villaluenga C, Rai DK, Birsan RI, Frias J, Martín-Diana AB (2020) Sprouted barley flour as a nutritious and functional ingredient. Foods 9(3):296. https://doi.org/10.3390/foods9030296
Salehi-Lisar SY, Bakhshayeshan-Agdam H (2016) Drought stress in plants: causes, consequences, and tolerance. In: Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran SP (eds) Drought stress tolerance in plants, vol 1. Springer, Cham, pp 1–16
Sallam A, Alqudah AM, Dawood MFA, Baenziger PS, Börner A (2019) Drought stress tolerance in wheat and barley: advances in physiology, breeding and genetics research. Int J Mol Sci 20(13):3137. https://doi.org/10.3390/ijms20133137
Seo T, Kurokawa R, Sato B (2012) A convenient method for determining the concentration of hydrogen in water: Use of methylene blue with colloidal platinum. Med Gas Res 2(1):1. https://doi.org/10.1186/2045-9912-2-1
Shi H, Ye T, Zhu JK, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65(15):4119–4131. https://doi.org/10.1093/jxb/eru184
Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28(1):66–80. https://doi.org/10.1007/s00344-008-9075-2
Wang Y, Duan X, Xu S, Wang R, Ouyang Z, Shen W (2016) Linking hydrogen-mediated boron toxicity tolerance with improvement of root elongation, water status and reactive oxygen species balance: a case study for rice. Ann Bot 118(7):1279–1291. https://doi.org/10.1093/aob/mcw181
Wang AG, Lou GH (1990) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol Commun 6:55–57. https://doi.org/10.13592/j.cnki.ppj.1990.06.031
Wang B, Bian B, Wang C, Li C, Fang H, Zhang J, Huang D, Huo J, Liao W (2019) Hydrogen gas promotes the adventitious rooting in cucumber under cadmium stress. PLoS ONE 14(2):e0212639. https://doi.org/10.1371/journal.pone.0212639
Wu Q, Su N, Chen Q, Shen W, Shen Z, Xia Y, Cui J (2015) Cadmium-induced hydrogen accumulation is involved in cadmium tolerance in Brassica campestris by reestablishment of reduced glutathione homeostasis. PLoS ONE 10(10):e0139956. https://doi.org/10.1371/journal.pone.0139956
Xie Y, Mao Y, Zhang W, Lai D, Wang Q, Shen W (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiol 165(2):759–773. https://doi.org/10.1104/pp.114.237925
Xu S, Zhu S, Jiang Y, Wang N, Wang R, Shen W, Yang J (2013) Hydrogen-rich water alleviates salt stress in rice during seed germination. Plant Soil 370(1–2):47–57. https://doi.org/10.1007/s11104-013-1614-3
Xu D, Cao H, Fang W, Pan J, Chen J, Zhang J, Shen W (2017a) Linking hydrogen-enhanced rice aluminum tolerance with the reestablishment of GA/ABA balance and miRNA-modulated gene expression: a case study on germination. Ecotoxicol Environ Saf 145:303–312. https://doi.org/10.1016/j.ecoenv.2017.07.055
Xu S, Jiang Y, Cui W, Jin Q, Zhang Y, Bu D, Fu J, Wang R, Zhou F, Shen W (2017b) Hydrogen enhances adaptation of rice seedlings to cold stress via the reestablishment of redox homeostasis mediated by miRNA expression. Plant Soil 414(1–2):53–67. https://doi.org/10.1007/s11104-016-3106-8
Zeng J, Zhang M, Sun X (2013) Molecular hydrogen is involved in phytohormone signaling and stress responses in plants. PLoS ONE 8(8):e71038. https://doi.org/10.1371/journal.pone.0071038
Zhang R, Li C, Fu K, Li C, Li C (2018a) Phosphorus alters starch morphology and gene expression related to starch biosynthesis and degradation in wheat grain. Front Plant Sci 8:2252. https://doi.org/10.3389/fpls.2017.02252
Zhang X, Su N, Jia L, Tian J, Li H, Huang L, Shen Z, Cui J (2018b) Transcriptome analysis of radish sprouts hypocotyls reveals the regulatory role of hydrogen-rich water in anthocyanin biosynthesis under UV-A. BMC Plant Biol 18:227. https://doi.org/10.1186/s12870-018-1449-4
Zhao M, Zhang H, Yan H, Qiu L, Baskin CC (2018) Mobilization and role of starch, protein, and fat reserves during seed germination of six wild grassland species. Front Plant Sci 9:234. https://doi.org/10.3389/fpls.2018.00234
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Acknowledgements
We gratefully acknowledge the provision of funds by China Agriculture Research System of MOF and MARA (CARS-05-19B).
Funding
Funding was supported by Agriculture Research System of China, (Grant no.CARS-05-19B ).
Author information
Authors and Affiliations
Contributions
Conceptualization: RS and JQ; experimental work: RS, XZ, CF, SZ, and LS; statistical analysis and critically review: RS and XZ; original draft preparation: XZ, RS; editing and content improvement: CF, SZ, LS, XZ, RS; supervision: JQ. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that no conflict of interest exists.
Additional information
Handling Editor: Nudrat Aisha Akram.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Song, R., Zhang, X., Feng, C. et al. Exogenous Hydrogen Promotes Germination and Seedling Establishment of Barley Under Drought Stress by Mediating the ASA-GSH Cycle and Sugar Metabolism. J Plant Growth Regul 42, 2749–2762 (2023). https://doi.org/10.1007/s00344-022-10742-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10742-x