Abstract
Cadmium (Cd) levels in agricultural soils are increasing because of industrial expansion and pesticide discharge. There are few plants that tolerate heavy metals particularly Cd. NaHS as hydrogen sulfide (H2S) donor plays a significant role in Cd tolerance by plants reducing its toxicity. The present research was oriented to evaluate the effect of NaHS in Cd and macro-/micronutrient uptake, as well as some physical and chemical parameters in Leucaena leucocephala plants exposed to this metal. Seedlings were grown in a hydroponic system and exposed to 5 ppm of Cd and NaHS at 1, 10, and 100 μM for 3 days. Inductively coupled plasma optical emission spectrometry (ICP/OES) was used to quantify Cd content and macro-/micronutrients in plant tissues. Results show a significant difference (Fisher’s LSD) in radicle length and chlorophyll but did not show effect on carotenoids content. Addition of NaHS to the media shows a significant increase in Cd uptake by root as NaHS concentration in media increased. The maximum Cd uptake (7670 ± 102 mg/kg) was found in the roots of plants exposed to 100 μM of NaHS. A significant reduction in catalase (CAT) activity was observed in the root system, which is due to Cd concentration inside tissues. Results suggested that NaHS helps to decrease the toxic effect of Cd on the growth and development of plants.
Graphical abstract
Similar content being viewed by others
References
Ali B, Tao O, Zhou Y, Gill R, Ali S, Rafiq M, Zhou W (2013) 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol Environ Saf 92:271–280. https://doi.org/10.1016/j.ecoenv.2013.02.006
Ali B, Gill R, Yang S, Gill M, Ali S, Rafiq M, Zhou W (2014a) Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotoxicol Environ Saf 110:197–207. https://doi.org/10.1016/j.ecoenv.2014.08.027
Ali B, Xu X, Gill R, Yang S, Ali S et al (2014b) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crops Prod 52:617–626. https://doi.org/10.1016/j.indcrop.2013.11.033
Asati A, Pichhode M, Nikhil K (2016) Effect of heavy metals on plants: an overview. IJAIEM 5(3):56–66. https://doi.org/10.13140/RG.2.2.27583.87204
Bertoli AC, Cannata MG, Carvalho R, Ribeiro AR, Freitas MP et al (2012) Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Ecotoxicol Environ Saf 86:176–181. https://doi.org/10.1016/j.ecoenv.2012.09.011
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78. https://doi.org/10.1016/j.niox.2014.02.005
Carpena R, Vázquez S, Esteban E, Fernández M, de Felipe M, Zornoza P (2003) Cadmium-stress in white lupin: effects on nodule structure and functioning. Plant Physiol Biochem 41(10):911–919. https://doi.org/10.1016/s09819428(03)00136-0
Chanu L, Gupta A (2016) Phytoremediation of lead using Ipomoea aquatica Forsk. In hydroponic solution. Chemosphere 156:407–411. https://doi.org/10.1016/j.chemosphere.2016.05.001
Chaoui A, El Ferjani E (2005) Effects of cadmium and copper on antioxidant capacities, lignification, and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. CR Biol 328(1):23–31. https://doi.org/10.1016/j.crvi.2004.10.001
Cluis C (2004) Junk-greedy greens: phytoremediation as a new option for soil decontamination. BioTeach J 2:61–67
Coakley S, Cahill G, Enright AM, O’Rourke B (2019) Cadmium hyperaccumulation and translocation in Impatiens glandulifera: From foe to friend? Sustainability 11(18):5018. https://doi.org/10.3390/su11185018
Corpas F, Palma J (2020) H2S signaling in plants and applications in agriculture. J Adv Res 24:131–137. https://doi.org/10.1016/j.jare.2020.03.011
Dawood M, Cao F, Jahangir M, 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
Dooley F, Nair S, Ward P (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS ONE 8(4):e62048. https://doi.org/10.1371/journal.pone.0062048
Folgar S, Torres E, Pérez M, Cid A, Herrero C, Abalde J (2009) Dunaliella salina as marine microalga highly tolerant to but a poor remover of cadmium. J Hazard Mater 165(1–3):486–493. https://doi.org/10.1016/j.jhazmat.2008.10.010
Fu M, Dawood M, Wang N, Wu F (2019) Exogenous hydrogen sulfide reduces cadmium uptake and alleviates cadmium toxicity in barley. Plant Growth Regul 89(2):227–237. https://doi.org/10.1007/s10725-019-00529-8
Gallego S, Benavides M, Tomaro M (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121(2):151–159. https://doi.org/10.1016/S0168-9452(96)04528-1
González-Velázquez J, Salas-Vázquez E, Flores-Tavizón E, López-Moreno M (2022) Effect of cadmium on macro and micronutrient uptake and translocation by Leucaena leucocephala. Bull Environ Contam Toxicol. https://doi.org/10.1007/s00128-022-03592-6
Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465(1–2):190–198. https://doi.org/10.1016/s0005-2736(00)00138-3
Guo T, Zhang G, Zhou M, Wu F, Chen J (2007) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17:505–512. https://doi.org/10.1016/s1002-0160(07)60060-5
Gupta D, Huang H, Nicoloso F, Schetinger M, Farias J et al (2013) Effect of Hg, As and Pb on biomass production, photosynthetic rate, nutrients uptake and phytochelatin induction in Pfaffia glomerata. Ecotoxicology 22(9):1403–1412. https://doi.org/10.1007/s10646-013-1126-1
Gutiérrez-Martínez P, Torres-Morán M, Romero-Puertas M, Casas-Solís J, Zarazúa-Villaseñor P, Sandoval-Pinto E et al (2020) Assessment of antioxidant enzymes in leaves and roots of Phaseolus vulgaris plants under cadmium stress. Biotecnia 22(2):110–118. https://doi.org/10.18633/biotecnia.v22i2.1252
Haider F, Liqun C, Coulter J, Cheema S, Wu J, Zhang T et al (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Helal H, Upenov A, Issa G (1999) Growth and uptake of Cd and Zn by Leucaena leucocephala in reclaimed soils as affected by NaCl salinity. J Plant Nutr Soil Sci 162(6):589–592. https://doi.org/10.1002/(SICI)1522-2624(199912)162:6%3c589::AID-JPLN589%3e3.0.CO;2-1
Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237(3):527–531. https://doi.org/10.1006/bbrc.1997.6878
Isaure M, Fayard B, Sarret G, Pairis S, Bourguignon J (2006) Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochim Acta B Atom Spectrosc 61(12):1242–1252. https://doi.org/10.1016/j.sab.2006.10.009
Kubier A, Wilkin R, Pichler T (2019) Cadmium in soils and groundwater: A review. Appl Geochem 108:104388. https://doi.org/10.1016/j.apgeochem.2019.104388
Li S, Yu J, Zhu M, Zhao F, Luan S (2012) Cadmium impairs ion homeostasis by altering K+ and Ca2+ channel activities in rice root hair cells. Plant Cell Environ 35:1998–2013. https://doi.org/10.1111/j.1365-3040,2012.02532.x
López M, Lugo L, Guzmán N, Álamo B (2016) Effect of cobalt ferrite (CoFe2O4) nanoparticles on the growth and development of Lycopersicon lycopersicum (tomato plants). Sci Total Environ 550:45–52. https://doi.org/10.1016/j.scitotenv.2016.01.063
López-Millán A, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65(2–3):376–385. https://doi.org/10.1016/j.envexpbot.2008.11.010
Luo S, Calderón-Urrea A, Yu J, Liao W, Xie J, Tang Z (2020) The role of hydrogen sulfide in plant alleviates heavy metal stress. Plant Soil 449(1):1–10. https://doi.org/10.1007/s11104-020-04471-x
Mahmud J, Hasanuzzaman M, Nahar K, Rahman A et al (2019) EDTA reduces cadmium toxicity in mustard (Brassica juncea L.) by enhancing metal chelation, antioxidant defense and glyoxalase systems. Acta Agrobot 72:1722. https://doi.org/10.5586/aa.1772
Mohamed A, Castagna A, Ranieri A, di Toppi S (2012) Cadmium tolerance in bras- sica juncea roots and shoots is affected by antioxidant status and phytochelatin bio-synthesis. Plant Physiol Biochem 57:15–22. https://doi.org/10.1016/j.plaphy.2012.05.002
Muhammad S, Iqbal MZ, Mohammad A (2008) Effect of lead and cadmium on germination and seedling growth of Leucaena leucocephala. JASEM 12(3):61–66. https://doi.org/10.4314/jasem.v12i3.55497
Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou W (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186(1):565–574. https://doi.org/10.1016/j.jhazmat.2010.11.037
Napoli A, Mason-Plunkett J, Valente J, Sucov A (2006) Full recovery of two simultaneous cases of hydrogen sulfide toxicity. Hosp Physician 42(5):47–50
Nazar R, Iqbal N, Masood A, Khan M, Syeed S, Khan N (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489. https://doi.org/10.4236/ajps.2012.310178
Nesler A, DalCorso G, Fasani E, Manara A et al (2017) Functional components of the bacterial CzcCBA efflux system reduce cadmium uptake and accumulation in transgenic tobacco plants. N Biotechnol 35:54–61. https://doi.org/10.1016/j.nbt.2016.11.006
Peralta-Videa J, Gardea-Torresdey J, Gómez E, Tiemann K, Parsons J, Carrillo G (2002) Effect of mixed cadmium, copper, nickel and zinc at different pHs upon alfalfa growth and heavy metal uptake. Environ Pollut 119(3):291–301. https://doi.org/10.1016/s0269-7491(02)00105-7
Pietrini F, Zacchini M, Iori V, Pietrosanti L, Bianconi D, Massacci A (2009) Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Int J Phytoremediation 12(1):105–120. https://doi.org/10.1080/15226510902767163
Piršelová B, Ondrušková E (2021) Effect of cadmium chloride and cadmium nitrate on growth and mineral nutrient content in the root of fava bean (Vicia faba L.). Plants 10:1007. https://doi.org/10.3390/plants10051007
Qian P, Sun R, Ali B, Gill R, Xu L, Zhou W (2014) Effects of hydrogen sulfide on growth, antioxidative capacity, and ultrastructural changes in oil seed rapeseedlings under aluminum toxicity. J Plant Growth Regul 33:526–538. https://doi.org/10.1007/s00344-013-9402-0
Qureshi M, Abdin M, Qadir S, Iqbal M (2007) Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plant 51:121–128. https://doi.org/10.1007/s10535-007-0024-x
Redondo S, Mateos E, Andrades L (2010) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum Macrostachyum. J Hazard Mater 184(1–3):299–307. https://doi.org/10.1016/j.jhazmat.2010.08.036
Rizwan M, Ali S, ur Rehman MZ, Rinklebe J, Tsang D, Bashir A et al (2018) Cadmium phytoremediation potential of brassica crop species: a review. Sci Total Environ 631–632:1175–1191. https://doi.org/10.1016/j.scitotenv.2018.03.104
Roberts T (2014) Cadmium and phosphorous fertilizers: the issues and the science. Procedia Eng 83:52–59. https://doi.org/10.1016/j.proeng.2014.09.012
Shani U, Ben-Gal A (2005) Long-term response of grapevines to salinity: osmotic effects and ion toxicity. Am Jof Enol Vitic 56(2):148–154
Sharma J, Chakraverty N (2013) Mechanism of plant tolerance in response to heavy metals. Physiol Mol Biol Plants. https://doi.org/10.1007/978-81-322-0807-5_12
Singh S, Singh A, Bashri G, Prasad S (2016) Impact of Cd stress on cellular functioning and its amelioration by phytohormones: An overview on regulatory network. Plant Growth Regul 80:253–263. https://doi.org/10.1007/s10725-016-0170-2
Sumanta N, Haque C, Nishika J, Suprakash R (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 4(9):63–69. https://doi.org/10.1055/s-0033-1340072
Takahashi R, Bashir K, Ishimaru Y, Nishizawa N, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607. https://doi.org/10.4161/psb.22454
Tao J, Lu L (2022) Advances in Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation in Plants. Toxics 10(8):411. https://doi.org/10.3390/toxics10080411
Tran T, Popova P (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37(1):1–13. https://doi.org/10.3906/bot-1112-16
US Environmental Protection Agency (1996) Ecological effects test guidelines. OPPTS 850.4200: seed germination/root elongation toxicity test. EPA 712712-C96–154, p 6
Yang Y, Zhang L, Huang X, Zhou Y, Quan Q, Li Y, Zhu X (2020) Response of photosynthesis to different concentrations of heavy metals in Davidia involucrate. PLoS ONE 15(3):e0228563. https://doi.org/10.1371/journal.pone.0228563
Yruela I (2009) Copper in plants: acquisition, transport and interaction. Funct Plant Biol 36(5):409–430. https://doi.org/10.1071/FP08288
Yu Y, Zhou X, Zhu Z, Zhou K (2019) Sodium hydrosulfide mitigates cadmium toxicity by promoting cadmium retention and inhibiting its translocation from roots to shoots in Brassica napus. J Agric Food Chem 67(1):433–440. https://doi.org/10.1021/acs.jafc.8b04622
Zhang H, Hu L, Hu K, He Y, Wang S, Luo J (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50(12):1518–1529. https://doi.org/10.1111/j.1744-7909.2008.00769.x
Acknowledgements
The authors acknowledge Mr. Delvis Pérez for providing access to the ICP-OES spectrometer at Tropical Agricultural Research Station (TARS) to carry out sample analysis. This research did not receive any specific Grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
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 (e.g. a society or other partner) 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
González-Velázquez, J., Salas-Vázquez, E. & López-Moreno, M.L. Effect of hydrogen sulfide on cadmium and macro- and micronutrients uptake by Leucaena leucocephala. Chem. Pap. 77, 5421–5430 (2023). https://doi.org/10.1007/s11696-023-02874-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11696-023-02874-5