Abstract
Contamination of agricultural soil by chromium (Cr) is a serious menace to environmental safety and global food security. Although potential of salicylic acid (SA) in mitigating heavy metal (HM) toxicity in plants is well recognized, detailed physiological mechanisms behind such beneficial effects under Cr-stress in tomato (Solanum lycopersicum L.) plant are far from being completely unravelled. The present study evaluated the efficacy of exogenously applied SA, in alleviating Cr-mediated alterations on photosynthesis and antioxidant defense in tomato exposed to three different concentrations of Cr(VI) [0, 50, and 100 mg Cr(VI) kg−1 soil]. Exposure of tomato plants to Cr resulted in increased Cr-accumulation and oxidative damage, as signposted by high Cr concentration in root as well as shoot, augmented malondialdehyde (MDA) and superoxides levels, and inhibition in enzymes of ascorbate–glutathione (AsA-GSH) cycle. Furthermore, a significant (P ≤ 0.05) reduction in photosynthetic pigments and gas exchange parameters was also evident in Cr-stressed tomato plants. Findings of the present study showed that exogenous application of 0.5 mM SA not only promoted plant growth subjected to Cr, but also restored Cr-mediated disturbances in plant physiology. A significant (P ≤ 0.05) decrease in Cr acquisition and translocation as evidenced by improved growth and photosynthesis in SA-treated plants was observed. Additionally, exogenous SA application by virtue of its positive effect on efficient antioxidant system ameliorated the Cr-mediated oxidative stress in tomato plants as signposted by lower MDA and superoxide levels and improved AsA-GSH cycle. Overall, current study advocates the potential of exogenous SA application in amelioration of Cr-mediated physiological disturbances in tomato plant.
Similar content being viewed by others
References
Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant MolBiol 69:451–462. https://doi.org/10.1007/s11103-008-9427-0
Adagunodo TA, SunmonuLA EME (2018) Heavy metals’ data in soils for agricultural activities. Data Brief 18:1847–1855
Agnihotri A, Seth CS (2016) Exogenously applied nitrate improves the photosynthetic performance and nitrogen metabolism in Tomato (Solanum lycopersicum L. cv. PusaRohini) under arsenic (V) toxicity. PhysiolMolBiol Plants 22:341–349. https://doi.org/10.1007/s12298-016-0370-2
Ahmad R, Ali S, Abid M, Rizwan M, Ali B, Tanveer A, Ahmad I, Azam M, Ghani MA (2020a) Glycinebetaine alleviates the chromium toxicity in Brassica oleracea L. by suppressing oxidative stress and modulating the plant morphology and photosynthetic attributes. Environ SciPollut Res 27:1101–1111. https://doi.org/10.1007/s11356-019-06761-z
Ahmad R, Ali S, Rizwan M, Dawood M, Farid M, Hussain A, Wijaya L, Alyemeni MN, Ahmad P (2020b) Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiol Plant 168(2):289–300
Ahmad R, Ali S, Rizwan M, Dawood M, Farid M, Hussain A, Wijaya L, Alyemeni MN, Ahmad P (2019) Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiol Plant 168:289–300. https://doi.org/10.1111/ppl.13001
Ali B (2017) Salicylic acid induced antioxidant system enhances the tolerance to aluminium in mung bean (Vigna radiata L. Wilczek) plants. Indian J Plant Physiol 22:178–189. https://doi.org/10.1007/s40502-017-0292-1
Ali S, Chaudhary A, Rizwan M, Anwar HT, Adrees M, Farid M, Irshad MK, Hayat T, Anjum SA (2015) Alleviation of Cr VI toxicity by glycinebetaine is related to elevated antioxidant enzymes and suppressed Cr VI uptake and oxidative stress in wheat (Triticum aestivum L.). Environ Sci Pollut Res 22:10669–10678. https://doi.org/10.1007/s11356-015-4193-4
Alloway BJ (ed) (2012) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability, vol 22. Springer Science & Business Media
Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles evidence for thermal dependence. Plant Physiol 98:501–508. https://doi.org/10.1104/pp.98.2.501
APHA, AWWA, WEF (2005) Standard methods for the examination of water and wastewater. 21st edn. Washington, DC
Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Azcue JM (1996) Comparison of different cleaning procedures of root material for analysis of trace elements. Int J Environ Anal Chem 62(2):137–145
Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaibi W, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicol Environ Saf 73(5):1004–1011
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Celma AR, Cuadros F, López-Rodríguez F (2009) Characterisation of industrial tomato by-products from infrared drying process. Food Bioproducts Process 87(4):282–291
Chen YY, Tang MY, Wang ST, Wang Q, Zhan WX, Huang G (2016) Evaluation of heavy metal pollution in farmland soil of China based on bibliometrics. Int J Phytoremediation 47:219–225
Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J ExpBot 63:5521–5534. https://doi.org/10.1093/jxb/ers201
El Dakak RA, Hassan IA (2020) The alleviative effects of salicylic acid on physiological indices and defense mechanisms of maize (Zea Mays L. Giza 2) stressed with cadmium. Environ Process 7:873–884. https://doi.org/10.1007/s40710-020-00448-1
Eleftheriou EP, Adamakis IDS, Panteris E, Fatsiou M (2015) Cr VI induced ultrastructural changes and oxidative stress in roots of Arabidopsis thaliana. Int J Mol Sci 16:15852–15871. https://doi.org/10.3390/ijms160715852
Farid M, Ali S, Saeed R, Rizwan M, Bukhari SAH, Abbasi GH, Hussain A, Ali B, Zamir MSI, Ahmad I (2019) Combined application of citric acid and 5-aminolevulinic acid improved biomass, photosynthesis and gas exchange attributes of sunflower (Helianthus annuus L.) grown on chromium contaminated soil. Int J Phytoremediation 21:760–767
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254. https://doi.org/10.1111/j.1399-3054.1997.tb04780.x
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Ganesh KS, Baskaran L, Rajasekaran S, Sumathi K, Chidambaram ALA, Sundaramoorthy P (2008) Cr VI stress induced alterations in biochemical and enzyme metabolism in aquatic and terrestrial plants. Colloids Surfaces B 63:159–163. https://doi.org/10.1016/j.colsurfb.2007.11.016
Gao Y, Xia J (2011) Chromium contamination accident in China: viewing environment policy of China. Environ Sci Technol 45(20):8605–8606. https://doi.org/10.1021/ES203101F
García-Caparrós P, De Filippis L, Gul A, Hasanuzzaman M, Ozturk M, Altay V, Lao MT (2020) Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. Bot Rev. https://doi.org/10.1007/s12229-020-09231-1
Global Tomato Industry Report 2020: Trends & Opportunities by Country, Consumption, Production, Price Developments, Imports and Exports (2007–2025).
Gomes MAD, Hauser-Davis RA, Suzuki MS, Vitória AP (2017) Plant chromium uptake and transport, physiological effects and recent advances in molecular investigations. Ecotoxicol Environ Saf 140:55–64
Gonzalez A, Mar Gil-Diaz M, Pinilla P, Carmen Lobo M (2017) Impact of Cr and Zn on Growth, Biochemical and Physiological Parameters, and Metal Accumulation by Wheat and Barley Plants. Water Air Soil Pollut 228:1–17. https://doi.org/10.1007/s11270-017-3507-1
Gordon LK, Minibayeva FV, Rakhmatullina DF, Alyabyev AJ, Ogorodnikova TI, Loseva NL, Valitova YN (2004) Heat production of wheat roots induced by the disruption of proton gradient by salicylic acid. Thermo Chimica Acta 422(1–2):101–104
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. FrontPlant Sci 6:171. https://doi.org/10.3389/fpls.2015.00171
Hiscox JT, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. https://doi.org/10.1139/b79-163
Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395. https://doi.org/10.1093/oxfordjournals.pcp.a076726
Hussain A, Ali S, Rizwan M (2018) Role of zinc-lysine on growth and chromium uptake in rice plants under Cr Stress. J Plant Growth Regul 37:1413–1422. https://doi.org/10.1007/s00344-018-9831-x
Islam F, Yasmeen T, Arif MS, Riaz M, Shahzad SM, Imran Q, Ali I (2016) Combined ability of chromium (Cr) tolerant plant growth promoting bacteria (PGPB) and salicylic acid (SA) in attenuation of chromium stress in maize plants. Plant Physiol Biochem 108:456–467. https://doi.org/10.1016/j.plaphy.2016.08.014
Kanagaraj G, Elango L (2019) Chromium and fluoride contamination in groundwater around leather tanning industries in southern India: implications from stable isotopic ratio δ53Cr/δ52Cr, geochemical and geostatistical modelling. Chemosphere 220:943–953. https://doi.org/10.1016/j.chemosphere.2018.12.105
Kazakis N, Kantiranis N, Kalaitzidou K, Kaprara E, Mitrakas M, Frei R, Vargemezis G, Tsourlos P, Zouboulis A, Filippidis A (2017) Origin of hexavalent chromium in groundwater: the example of Sarigkiol Basin. Northern Greece Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2017.03.128
Kohli SK, Handa N, Kaur R, Kumar V, Khanna K, Bakshi P, Singh R, Arora S, Kaur R, Bhardwaj R (2017) Role of Salicylic Acid in Heavy Metal Stress Tolerance: Insight into Underlying Mechanism. In: Nazar R, Iqbal N, Khan NA (eds) Salicylic Acid: A Multifaceted Hormone 2017. Springer, Singapore, pp 123–144. https://doi.org/10.1007/978-981-10-6068-7
Kumar P, Tokas J, Singal HR (2019) Amelioration of chromium VI toxicity in sorghum (Sorghum bicolor L.) using glycine betaine. Sci Rep 9(1):1–15
Liu Z, Ding Y, Wang F, Ye Y, Zhu C (2016) Role of SA in resistance to cadmium stress in plants. Plant Cell Rep 35:719–731. https://doi.org/10.1007/s00299-015-1925-3
Lu Q, Zhang T, Zhang W, Su C, Yang Y, Hu D, Xu Q (2018) Alleviation of cadmium toxicity in Lemna minor by exogenous salicylic acid. Ecotoxicol Environ Saf 147:500–508. https://doi.org/10.1016/j.ecoenv.2017.09.015
Ma J, Lv C, Xu M, Chen G, Lv C, Gao Z (2016) Photosynthesis performance antioxidant enzymes and ultrastructural analyses of rice seedlings under Cr VI stress. Environ Sci Pollut Res 23:1768–1778. https://doi.org/10.1007/s11356-015-5439-x
Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) γ-aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26:675–690. https://doi.org/10.1007/s10646-017-1800-9
Metwally AM, Radi AA, El-Shazoly RM, Hamada AM (2018) The role of calcium, silicon and salicylic acid treatment in protection of canola plants against boron toxicity stress. J Plant Res 22:1–4. https://doi.org/10.1007/s10265-018-1008
Mohamed HI, El-Shazly HH, Badr A (2020) Role of Salicylic Acid in Biotic and Abiotic Stress Tolerance in Plants. In: Lone R, Shuab R, Kamili AN (eds) Plant Phenolics in Sustainable Agriculture. Springer, Singapore, pp 533–554. https://doi.org/10.1007/978-981-15-4890-1_23
Moral R, Pedreno JN, Gomez I, Mataix J (1995) Effects of chromium on the nutrient element content and morphology of tomato. J Plant Nutr 18(4):815–822
Moustafa-Farag M, Mahmoud HI, Mahmoud A, Elkelish A, Misra AN, Guy KM, Kamran M, Ai S, Zhang M (2020) Salicylic acid stimulates antioxidant defense and osmolyte metabolism to alleviate oxidative stress in watermelons under excess boron. Plants 9:724. https://doi.org/10.3390/plants9060724
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nguyen TQ, Sesin V, Kisiala A, Emery RN (2021) Phytohormonal roles in plant responses to heavy metal stress: implications for using macrophytes in phytoremediation of aquatic ecosystems. Environ Toxicol Chem 40:7–22
Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160. https://doi.org/10.1111/pce.12726
Palmgren MG, Harper JF (1999) Pumping with plant P-type ATPases. J Exp Botany 50:883–893
Rebhi AE, Lounici H, Lahrech MB, Morel JL (2019) Response of Artemisia herba alba to hexavalent chromium pollution under arid and semi-arid conditions. Int J Phytoremediation 21:224–229. https://doi.org/10.1080/15226514.2018.1524841
Sameena PP, Puthur JT (2021) Cotyledonary leaves effectively shield the true leaves in Ricinuscommunis L. from copper toxicity. Int J Phytoremed 23:492–504
Sarath NG, Puthur JT (2020) Heavy metal pollution assessment in a mangrove ecosystem scheduled as a community reserve. Wetlands Ecol Manage. https://doi.org/10.1007/s11273-020-09764-7
Shackira AM, Jazeel K, Puthur JT (2021) Phycoremediation and phytoremediation: Promising tools of green remediation. In: Mishra V, Kumar A (eds) Sustainable Environmental Clean-up (pp. 273–293). Elsevier
Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533
Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS (2020) Chromium bioaccumulation and its impacts on plants: an overview. Plants 9:100. https://doi.org/10.3390/plants9010100
Shen Y, Li J, Gu R, Yue L, Wang H, Zhan X, Xing B (2018) Carotenoid and superoxide dismutase are the most effective antioxidants participating in ROS scavenging in phenanthrene accumulated wheat leaf. Chemosphere 197:513–525. https://doi.org/10.1016/j.chemosphere.2018.01.036
Sihag S, Brar B, Joshi UN (2019) Salicylic acid induces amelioration of chromium toxicity and affects antioxidant enzyme activity in Sorghum bicolor L. Int J Phytoremed 21:293–304. https://doi.org/10.1080/15226514.2018.1524827
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016a) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143
Singh VP, Kumar J, Singh M, Singh S, Prasad SM, Dwivedi R, Singh MPVVB (2016b) Role of salicylic acid-seed priming in the regulation of chromium(VI) and UV-B toxicity in maize seedlings. Plant Growth Regul 78:79–91. https://doi.org/10.1007/s10725-015-0076-4
Singh D, Sharma NL, Singh CK, Sarkar SK, Singh I, Dotaniya ML (2020) Effect of chromium (VI) toxicity on morpho-physiological characteristics, yield, and yield components of two chickpea (Cicer arietinum L.) varieties. PLoS ONE 15(12):e0243032
Srivastava D, Tiwari M, Dutta P, Singh P, Chawda K, Kumari M, Chakrabarty D (2021) Chromium stress in plants: toxicity. Tolerance Phytoremed Sustain 13(9):4629
Sumalan RM, Ciulca SI, Poiana MA, Moigradean D, Radulov I, Negrea M, Sumalan RL (2020) The antioxidant profile evaluation of some tomato Landraces with soil salinity tolerance correlated with high nutraceuticaland functional value. Agronomy 10:500
Tan S, Ke Z, Chai D, Miao Y, Luo K, Li W (2021) Lycopene, polyphenols and antioxidant activities of three characteristic tomato cultivars subjected to two drying methods. Food Chem 338:128062
Tumolo M, Ancona V, De Paola D, Losacco D, Campanale C, Massarelli C, Uricchio VF (2020) Chromium pollution in european water, sources, health risk, and remediation strategies: an overview. Int J Env Res Pub He 17:5438. https://doi.org/10.3390/ijerph17155438
Wakeel A, Xu M, Gan Y (2020) Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int J MolSci 21:728. https://doi.org/10.3390/ijms21030728
Wu QS, Zou YN, Xia RX (2006) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine L.) roots. Eur J Soil Biol 42:166–172. https://doi.org/10.1016/j.ejsobi.2005.12.006
Yuan L, Shu S, Sun J, Guo S, Tezuka T (2012) Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system and chloroplast ultrastructure in Cucumis sativus L under Ca(NO3)2 stress. Photosynth Res 112:205–214. https://doi.org/10.1007/s11120-012-9774-1
Zewail RM, El-DesoukeyHS IKR (2020) Chromium stress alleviation by salicylic acid in Malabar spinach (Basella alba). J Plant Nutri 43:1268–1285
Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through up-regulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924. https://doi.org/10.1007/s00709-014-0732-y
Ziegler RG, Vogt TM (2002) Tomatoes, lycopene, and risk of prostate cancer. Pharmaceutical Biol 40:59–69
Acknowledgements
The authors are thankful to Head, Department of Botany, University of Delhi for providing the research facilities. Mr. Ashish Agnihotri, Ph.D. scholar is deeply apprecited for his crucial contribution in revising this manuscript. The Institution of Eminence (IoE), University of Delhi is greatly acknowledged for providing the assistance in the research.
Author information
Authors and Affiliations
Contributions
Samta Gupta: Performing, collection and assembly of the data, analysis and interpretation of the data, drafting and writing the manuscript, statistical analysis. Chandra Shekhar Seth: Conception and design of the experiment, critical revision of the article for important intellectual content, final approval of the article, provision of study materials, experimental expertise, obtaining of funding, administrative, technical, or logistic support.
Corresponding author
Ethics declarations
Conflicts of interest
All authors declare that they have no conflicts of interest.
Consent to participate
Yes.
Consent for publication
Yes.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gupta, S., Seth, C.S. Salicylic acid alleviates chromium (VI) toxicity by restricting its uptake, improving photosynthesis and augmenting antioxidant defense in Solanum lycopersicum L. Physiol Mol Biol Plants 27, 2651–2664 (2021). https://doi.org/10.1007/s12298-021-01088-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-01088-x