Abstract
Cadmium (Cd) is a poisonous element for human health. This study was conducted to explore whether H2S can alleviate the toxic effects of Cd on ginger. Specifically, ginger plants were grown in soil and treated with 7.5 mg·l−1 CdCl2, after which water (T1), 0.8 mM NaHS (T2), or 0.8 mM NaHS and 0.15 mM HT (T3) were added to the soil. The application of NaHS increased the activities of antioxidant enzymes (APX, GR, MDHAR, and DHAR) during the early treatment stage. It also inhibited the decrease in Pn, Gs, and Ls under Cd stress conditions while also limiting the increase in Ci. An analysis of the expression of Cd uptake-related genes indicated that NaHS upregulated the expression of ZoNramp1, which encodes a metal transporter, in roots as well as ZoPCS1, which encodes a phytochelatin synthase. In contrast, NaHS downregulated ZoHMA2 expression in the rhizomes and roots under Cd stress conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- HT:
-
Hypotaurine
References
Ali S, Farooq MA, Yasmeen T, Hussain S, Arif MS et al (2013) The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. Ecotoxicol Environ Saf 89:66–72. https://doi.org/10.1016/j.ecoenv.2012.11.015
Cao B, Ma Q, Zhao Q, Wang L, Xu K (2015) Effects of silicon on absorbed light allocation, antioxidant enzymes and ultrastructure of chloroplasts in tomato leaves under simulated drought stress. Sci Hortic 194:53–62. https://doi.org/10.1016/j.scienta.2015.07.037
Chao DP, Tyan CC, Chen JJ, Hsieh CL, Sheen LY (2011) Effect of hot-attribute aged ginger tea on Chinese medical pulse condition of healthy young humans. J Tradit Complement Med 1:69–75. https://doi.org/10.1016/s2225-4110(16)30059-1
Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH et al (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493. https://doi.org/10.1093/jxb/err145
Chen Z, Xu J, Xu Y, Wang K, Cao B et al (2019) Alleviating effects of silicate, selenium, and microorganism fertilization on lead toxicity in ginger (Zingiber officinale Roscoe). Plant Physiol Biochem 145:153–163. https://doi.org/10.1016/j.plaphy.2019.10.027
Cheng W, Zhang L, Jiao C, Su M, Yang T et al (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286. https://doi.org/10.1016/j.plaphy.2013.05.042
Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128. https://doi.org/10.1016/j.jhazmat.2011.12.076
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. Cv. Azad). J Exp Bot 52:1101–1109. https://doi.org/10.1093/jexbot/52.358.1101
Fang H, Jing T, Liu Z, Zhang L, Jin Z et al (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481. https://doi.org/10.1016/j.ceca.2014.10.004
Franck T, Kevers C, Gaspar T (1995) Protective enzymatic systems against activated oxygen species compared in normal and vitrified shoots of Prunus avium L. raised in vitro. Plant Growth Regul 16:253–256. https://doi.org/10.1007/BF00024782
Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol Plant 160:396–409. https://doi.org/10.1111/ppl.12581
Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W et al (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420. https://doi.org/10.3389/fpls.2015.00420
Jin Z, Shen J, Qiao Z, Yang G, Wang R et al (2011) Hydrogen sulfide improves drought resistance in arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486. https://doi.org/10.1016/j.bbrc.2011.09.090
Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P (2020) Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) Plants to iron deficiency and salt stress alone or in combination. Physiol Plant 168:256–277. https://doi.org/10.1111/ppl.12976
Kikuchi T, Okazaki M, Kimura SD, Motobayashi T, Baasansuren J et al (2008) Suppressive effects of magnesium oxide materials on cadmium uptake and accumulation into rice grains: II: suppression of cadmium uptake and accumulation into rice grains due to application of magnesium oxide materials. J Hazard Mater 154:294–299. https://doi.org/10.1016/j.jhazmat.2007.10.025
Kushwaha BK, Singh VP (2020) Glutathione and hydrogen sulfide are required for sulfur-mediated mitigation of Cr(VI) toxicity in tomato, pea and brinjal seedlings. Physiol Plant 168:406–421. https://doi.org/10.1111/ppl.13024
Li H, Wang Y, Xiao J, Xu K (2015) Reduced photosynthetic dark reaction triggered by aba application increases intercellular Co2 concentration, generates H2O2 and promotes closure of stomata in ginger leaves. Environ Exp Bot 113:11–17. https://doi.org/10.1016/j.envexpbot.2015.01.002
Li H, Zhang Y, Xiao J, Xu K (2013) Photosynthetic dark reaction is more sensitive to ABA signalling caused by osmotic stress than Ca2+ signalling in ginger leaves. Sci Hortic 164:73–76. https://doi.org/10.1016/j.scienta.2013.09.003
Li L, Wang Y, Shen W (2012a) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631. https://doi.org/10.1007/s10534-012-9551-9
Li R, Luo X, Zhu Y, Zhao L, Li L et al (2017) ATM signals to AMPK to promote autophagy and positively regulate DNA damage in response to cadmium-induced ROS in mouse spermatocytes. Environ Pollut 231:1560–1568. https://doi.org/10.1016/j.envpol.2017.09.044
Li X, Gong B, Xu K (2014) Interaction of nitric oxide and polyamines involves antioxidants and physiological strategies against chilling-induced oxidative damage in Zingiber officinale Roscoe. Sci Hortic 170:237–248. https://doi.org/10.1016/j.scienta.2014.03.026
Li ZG, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca(2+) and calmodulin. Plant Sci 185–186:185–189. https://doi.org/10.1016/j.plantsci.2011.10.006
Lindblad AJ, Koppula S (2016) Ginger for nausea and vomiting of pregnancy. Can Fam Physician 62:145
Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K et al (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935. https://doi.org/10.1016/j.plaphy.2010.09.016
Liu ZJ, Guo YK, Bai JG (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two Cucumber ecotypes under osmotic stress. J Plant Growth Regul 29(2):171–183
Martin SR, Llugany M, Barceló J, Poschenrieder C (2012) Cadmium exclusion a key factor in differential Cd-resistance in Thlaspi arvense ecotypes. Biol Plant 56:729–734. https://doi.org/10.1007/s10535-012-0056-8
Mostofa MG, Rahman A, Ansary MM, Watanabe A, Fujita M et al (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078. https://doi.org/10.1038/srep14078
Nakamura M, Kuramata M, Kasugai I, Abe M, Youssefian S (2009) Increased thiol biosynthesis of transgenic poplar expressing a wheat o-acetylserine(thiol) lyase enhances resistance to hydrogen sulfide and sulfur dioxide toxicity. Plant Cell Rep 28:313–323. https://doi.org/10.1007/s00299-008-0635-5
Pormehr M, Ghanati F, Sharifi M, McCabe PF, Hosseinkhani S et al (2019) The role of SIPK signaling pathway in antioxidant activity and programmed cell death of tobacco cells after exposure to cadmium. Plant Sci 280:416–423. https://doi.org/10.1016/j.plantsci.2018.12.028
Rauckman EJ, Rosen GM, Kitchell BB (1979) Superoxide radical as an intermediate in the oxidation of hydroxylamines by mixed function amine oxidase. Mol Pharmacol 15:131–137
Rizwan M, Mostofa MG, Ahmad MZ, Zhou Y, Adeel M et al (2019) Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel. Plant Physiol Biochem 138:100–111. https://doi.org/10.1016/j.plaphy.2019.02.023
Roldán A, Díaz-Vivancos P, Hernández JA, Carrasco L, Caravaca F (2008) Superoxide dismutase and total peroxidase activities in relation to drought recovery performance of mycorrhizal shrub seedlings grown in an amended semiarid soil. J Plant Physiol 165:715–722. https://doi.org/10.1016/j.jplph.2007.02.007
Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M et al (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44. https://doi.org/10.1007/978-3-319-06746-9_1
Shim D, Hwang JU, Lee J, Lee S, Choi Y et al (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21:4031–4043. https://doi.org/10.1105/tpc.109.066902
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372. https://doi.org/10.1016/j.pbi.2009.05.001
Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) Seedlings. Planta 231:1301–1309. https://doi.org/10.1007/s00425-010-1134-9
Wang L, Gao F, Xu K, Li X (2014) Natural occurrence of mixploid ginger (Zingiber officinale Rosc.) In China and its morphological variations. Sci Hortic 172:54–60. https://doi.org/10.1016/j.scienta.2014.03.043
Wang Y, Li L, Cui W, Xu S, Shen W et al (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119. https://doi.org/10.1007/s11104-011-0936-2
Xie Y, Zhang C, Lai D, Sun Y, Samma MK et al (2014) Hydrogen sulfide delays Ga-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53–62. https://doi.org/10.1016/j.jplph.2013.09.018
Yang G (2011) Hydrogen sulfide in cell survival: a double-edged sword. Expert Rev Clin Pharmacol 4:33–47. https://doi.org/10.1586/ecp.10.131
Yin F, Liu X, Cao B, Xu K (2020) Low Ph altered salt stress in antioxidant metabolism and nitrogen assimilation in ginger (Zingiber officinale) seedlings. Physiol Plant 168:648–659. https://doi.org/10.1111/ppl.13011
Zhan K, Xu K, Yin H (2011) Preparative separation and purification of gingerols from ginger (Zingiber officinale Roscoe) by high-speed counter-current chromatography. Food Chem 126:1959–1963. https://doi.org/10.1016/j.foodchem.2010.12.052
Zhang H, Hu LY, Hu KD, He YD, Wang SH et al (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529. https://doi.org/10.1111/j.1744-7909.2008.00769.x
Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP et al (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567. https://doi.org/10.1111/j.1744-7909.2010.00946.x
Funding
This study was supported by the National Characteristic Vegetable Industry Technology System Project (Grant No. CARS-24-A-09), the Taishan Industrial Experts Program, China (Grant No. tscy20190105), and the project of Agricultural Excellent Germplasm in Shan Dong Province (Grant No. 2020LZGC006).
Author information
Authors and Affiliations
Contributions
Data curation: Zijing Chen. Investigation: Canyu Liu. Resources: Kun Xu. Software: Bili Cao. Writing – original draft: Zijing Chen. Writing – review and editing: Kun Xu.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Gangrong Shi
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Zijing Chen and Canyu Liu contributed equally to this paper.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, Z., Liu, C., Cao, B. et al. A hydrogen sulfide application can alleviate the toxic effects of cadmium on ginger (Zingiber officinale Roscoe). Environ Sci Pollut Res 29, 68422–68431 (2022). https://doi.org/10.1007/s11356-022-20635-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-20635-x