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Methyl jasmonate and selenium synergistically mitigative cadmium toxicity in hot pepper (Capsicum annuum L.) plants by improving antioxidase activities and reducing Cd accumulation

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Abstract

Methyl jasmonate (MeJA) or selenium (Se)-mediated response to cadmium (Cd) stress in plant has been widely reported, but the combined effects both on plant growth in response to Cd stress and the underlying mechanisms remain obscure. Here, we showed the combined effects of MeJA (2.5 μM) and Se (7 μM) on hot pepper growth under Cd stress (CdCl2, 5 μM). The results showed Cd suppressed the accumulation of total chlorophyll and carotenoid and reduced the photosynthesis, while it increased the content of endogenous signaling molecules, e.g. nitric oxide (NO) and hydrogen peroxide (H2O2), as well as Cd content in leaves. The combined application of MeJA and Se significantly decreased the malondialdehyde (MDA) accumulation and improved the activities of antioxidant enzymes (AOEs, e.g. SOD and CAT) and defense-related enzymes (DREs, POD and PAL). Additionally, the synergistic application of MeJA and Se also obviously improved photosynthesis in hot pepper plants under Cd stress compared with those treated with MeJA or Se respectively or not. Moreover, the treatment of MeJA associated with Se also effectively reduced the Cd accumulation in hot pepper leaves under Cd stress compared with the plants treated with MeJA or Se separately, which implied a potentially synergistic role of MeJA and Se in alleviating Cd toxicity in hot pepper plants. This study provides a theoretical reference for the further analysis of the molecular mechanism of MeJA and Se in jointly mediating the response to heavy metals in plants.

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References

  • Ahmad R, Waraich EA, Nawaz F, Ashraf MY, Khalid M (2016) Selenium (Se) improves drought tolerance in crop plants–a myth or fact? J Sci Food Agric 96:372–380

    CAS  Google Scholar 

  • Amani S, Mohebodini M, Khademvatan S, Jafari M (2020) Agrobacterium rhizogenes mediated transformation of Ficus carica L. for the efficient production of secondary metabolites. J Sci Food Agr 100:2185–2197

    CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22:17022–17030

    CAS  Google Scholar 

  • Baruah N, Subham CM, Farooq M, Gogoi N (2019) Influence of heavy metals on seed germination and seedling growth of wheat, pea, and tomato. Water Air Soil Pollut 230:273–288

    CAS  Google Scholar 

  • Basit F, Tao J, An J (2023) Nitric oxide and brassinosteroids enhance chromium stress tolerance in Glycine max L. (Merr.) by modulating antioxidative defense and glyoxalase systems. Environ Sci Pollut Res Int 30(18):51638–51653

    CAS  Google Scholar 

  • Byrne SL, Durandeau K, Nagy I, Barth S (2010) Identification of ABC transporters from Lolium perenne L. that are regulated by toxic levels of selenium. Planta 231:901–911

    CAS  Google Scholar 

  • Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356

    CAS  Google Scholar 

  • Cheng Y, Li X, Fang MY, Ye QJ, Li ZM, Ahammed GJ (2022) Systemic H2O2 signaling mediates epigallocatechin-3-gallate-induced cadmium tolerance in tomato. J Hazard Mater 438:129511

    CAS  Google Scholar 

  • Dai Z, Yuan Y, Huang H, Hossain MM, Xiong S, Cao M, Ma LQ, Tu S (2021) Methyl jasmonate mitigates high selenium damage of rice via altering antioxidant capacity, selenium transportation and gene expression. Sci Total Environ 756:143848

    CAS  Google Scholar 

  • Dinh QT, Wang MK, Tran TAT, Zhou F, Wang D, Zhai H, Peng Q, Xue MY, Du ZK, Banuelos GS, Lin ZQ, Liang DL (2019) Bioavailability of selenium in soil-plant system and a regulatory approach. Crit Rev Env Sci Tec 49:443–517

    CAS  Google Scholar 

  • Feng R, Zhao P, Zhu Y, Yang J, Wei X, Yang L, Liu H, Rensing C, Ding Y (2021) Application of inorganic selenium to reduce accumulation and toxicity of heavy metals (metalloids) in plants: the main mechanisms, concerns, and risks. Sci Total Environ 771:144776

    CAS  Google Scholar 

  • Ferrer-Sueta G, Vitturi D, Batinic-Haberle I, Fridovich I, Goldstein S, Czapski G, Radi R (2003) Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion. J Biol Chem 278:27432–27438

    CAS  Google Scholar 

  • Filek M, Gzyl-Malcherc B, Zembala M, Bednarska E, Laggner P, Kriechbaum M (2010) Effect of selenium on characteristics of rape chloroplasts modified by cadmium. J Plant Physiol 167:28–33

    CAS  Google Scholar 

  • Filipiak-Szok A, Kurzawa M, Szłyk E (2015) Determination of toxic metals by ICP-MS in Asiatic and European medicinal plants and dietary supplements. J Trace Elem Med Biol 30:54–58

    CAS  Google Scholar 

  • Friberg LT, Elinder GG, Kjellstrom T, Nordberg GF (Eds.) (2019) Cadmium and health: a toxicological and epidemiological appraisal: Volume 2: Effects and response (Vol. 1); CRC Press: Boca Raton

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    CAS  Google Scholar 

  • Ghorbani A, Pishkar L, Roodbari N, Ali Tavakoli S, Moein Jahromi E, Chu W (2023) Nitrate reductase is needed for methyl jasmonate-mediated arsenic toxicity tolerance of rice by modulating the antioxidant defense system, glyoxalase system and arsenic sequestration mechanism. J Plant Growth Regul 42:1107–1119

    CAS  Google Scholar 

  • Jiang H, Lin W, Jiao H, Liu J, Chan L, Liu X, Wang R, Chen T (2021) Uptake, transport, and metabolism of selenium and its protective effects against toxic metals in plants: a review. Metallomics 13:mfab040

    Google Scholar 

  • Kanu AS, Ashraf U, Mansaray LR, Abbas F, Fiaz S, Amanullah S, Charley CS, Tang X (2022) Exogenous methyl jasmonate application improved physio-biochemical attributes, yield, quality, and Cadmium tolerance in fragrant rice. Front Plant Sci 13:849477

    Google Scholar 

  • Kaur N, Sharma S, Kaur S, Nayyar H (2014) Selenium in agriculture: a nutrient or contaminant for crops? Arch Agron Soil Sci 60:1593–1624

  • Kaushik S, Sharma P, Kaur G, Singh AK, Al-Misned FA, Shafik HM, Sirhindi G (2022) Seed priming with methyl jasmonate mitigates copper and cadmium toxicity by modifying biochemical attributes and antioxidants in Cajanus cajan. Saudi J Biol Sci 29:721–729

    CAS  Google Scholar 

  • Kaya C, Ugurlar F, Ashraf M, Noureldeen A, Darwish H, Ahmad P (2021c) Methyl jasmonate and sodium nitroprusside jointly alleviate Cadmium toxicity in wheat (Triticum aestivum L.) plants by modifying nitrogen metabolism, Cadmium detoxification, and AsA-GSH cycle. Front Plant Sci 12:654780

    Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    CAS  Google Scholar 

  • Li H, Liu X, Wassie M, Chen L (2020) Selenium supplementation alleviates cadmium-induced damages in tall fescue through modulating antioxidant system, photosynthesis efficiency, and gene expression. Environ Sci Pollut Res Int 27:9490–9502

    CAS  Google Scholar 

  • Lin L, Zhou W, Dai H, Cao F, Zhang G, Wu F (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235–236:343–351

    Google Scholar 

  • Liu M, Sun J, Li Y, Xiao Y (2017) Nitrogen fertilizer enhances growth and nutrient uptake of Medicago sativa inoculated with Glomus tortuosum grown in Cd contaminated acidic soil. Chemosphere 167:204–211

    CAS  Google Scholar 

  • Luyckx M, Hausman JF, Sergeant K, Guerriero G, Lutts S (2021) Molecular and biochemical insights into early responses of hemp to Cd and Zn exposure and the potential effect of Si on stress response. Front Plant Sci 12:711853

    Google Scholar 

  • Malka M, Laing GD, Bohn T (2022) Separate effects of foliar applied Selenate and Zinc Oxide on the accumulation of macrominerals, macronutrients and bioactive compounds in two pea (Pisum sativum L.) seed varieties. Plants (Basel) 11:2009

    CAS  Google Scholar 

  • Manzoor HM, Bukhat S, Rasul S, Rehmani MIA, Noreen S, Athar HU, Zafar ZU, Skalicky M, Soufan W, Brestic M, Habib-Ur-Rahman M, Ogbaga CC, El Sabagh A (2022) Methyl jasmonate alleviated the adverse effects of Cadmium stress in pea (Pisum sativum L): a nexus of photosystem II activity and dynamics of redox balance. Front Plant Sci 13:860664

    Google Scholar 

  • Moreno-Escamilla JO, Alvarez-Parrilla E, de la Rosa LA, Núñez-Gastélum JA, González-Aguilar GA, Rodrigo-García J (2017) Effect of different elicitors and preharvest day application on the content of phytochemicals and antioxidant activity of butterhead lettuce (Lactuca sativa var. capitata) produced under hydroponic conditions. J Agric Food Chem 65:5244–5254

    CAS  Google Scholar 

  • Mozafariyan M, Shekari L, Hawrylak-Nowak B, Kamelmanesh MM (2014) Protective role of Selenium on pepper exposed to Cadmium stress during reproductive stage. Biol Trace Elem Res 160:97–107

    CAS  Google Scholar 

  • Nandagopal JGT, Harinarayanan UND, Raghavan S, Girija S (2022) Foliar selenium application mitigates low-temperature stress in chilli (Capsicum annuum L.) seedlings. Energy Nexus 6:100079

    CAS  Google Scholar 

  • Perez-Millan R, Alfosea-Simon M, Zavala-Gonzalez EA, Camara-Zapata JM, Martinez-Nicolas JJ, Lidon V, Simon I, Shahid MA, Garcia-Sanchez F, Simon-Grao S (2021) The addition of Selenium to the nutrient solution decreases Cadmium toxicity in pepper plants grown under hydroponic conditions. Agronomy 11:1905

    CAS  Google Scholar 

  • Rathinapriya P, Pandian S, Rakkammal K, Balasangeetha M, Alexpandi R, Satish L, Rameshkumar R, Ramesh M (2020) The protective effects of polyamines on salinity stress tolerance in foxtail millet (Setaria italica L.), an important C4 model crop. Physiol Mol Biol Plants 26:1815–1829

    CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544

    Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243

    Google Scholar 

  • Saidi I, Chtourou Y, Djebali W (2014) Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171:85–91

    CAS  Google Scholar 

  • Sams CE, Panthee DR, Charron CS, Kopsell DA, Yuan JS (2011) Selenium regulates gene expression for glucosinolate and carotenoid biosynthesis in Arabidopsis. J Am Soc Hortic Sci 136:23–34

    CAS  Google Scholar 

  • Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavymetal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. In: Whitacre D (ed) Reviews of environmental contamination and toxicology volume 232. Reviews of environmental contamination and toxicology (Continuation of Residue Reviews), vol 232. Springer, Cham

    Google Scholar 

  • Shang J, Gong H, Zhang Q, Cui Z, Li S, Lv P, Pan T, Ge Y, Qi Z (2021) The dynamic covalent reaction based on diselenide-containing crown ether irradiated by visible light. Chin Chem Lett 32(6):2005–2008

    CAS  Google Scholar 

  • Singh I, Shah K (2014) Exogenous application of methyl jasmonate lowers the effect of Cadmium-induced oxidative injury in rice seedlings. Phytochemistry 108:57–66

    CAS  Google Scholar 

  • Singh P, Arif Y, Miszczuk E, Bajguz A, Hayat S (2022) Specific roles of lipoxygenases in development and responses to stress in plants. Plants 11:979

    CAS  Google Scholar 

  • Srinivasan K (2016) Biological activities of red pepper (Capsicum annuum) and its pungent principle capsaicin: a review. Crit Rev Food Sci Nutr 56:1488–1500

    CAS  Google Scholar 

  • Tian SL, Khan A, Zheng WN, Song L, Liu JH, Wang XQ, Li L (2022) Effects of Chlorella extracts on growth of Capsicum annuum L. seedlings. Sci. Rep.-Uk 12:15455

    CAS  Google Scholar 

  • Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Google Scholar 

  • Turakainen M, Hartikainen H, Seppanen MM (2004) Effects of selenium treatments on potato (Solanum tuberosum L.) growth and concentrations of soluble sugars and starch. J Agric Food Chem 52:5378–5382

    CAS  Google Scholar 

  • Wang Z, Li Q, Wu W, Guo J, Yang Y (2017) Cadmium stress tolerance in wheat seedlings induced by ascorbic acid was mediated by NO signaling pathways. Ecotoxicol Environ Saf 135:75–81

    CAS  Google Scholar 

  • Wei T, Li X, Yashir N, Li H, Sun Y, Hua L, Ren X, Guo J (2021) Effect of exogenous silicon and methyl jasmonate on the alleviation of cadmium-induced phytotoxicity in tomato plants. Environ Sci Pollut Res Int 28:51854–51864

    CAS  Google Scholar 

  • Wu Z, Yin X, Bañuelos GS, Lin ZQ, Zhu Z, Liu Y, Yuan L, Li M (2016) Effect of selenium on control of postharvest gray mold of tomato fruit and the possible mechanisms involved. Front Microbiol 6:1441

    Google Scholar 

  • Wu X, Song H, Guan C, Zhang Z (2020) Boron mitigates cadmium toxicity to rapeseed (Brassica napus) shoots by relieving oxidative stress and enhancing cadmium chelation onto cell walls. Environ Pollut 263:114546

    CAS  Google Scholar 

  • Xiao XR, Shao ZF, Yu L (2021) A perspective of the engineering applications of carbon-based selenium-containing materials. Chin Chem Lett 32(10):2933–2938

    CAS  Google Scholar 

  • Xu YK, Tao GD, Liu HM, Yan KL, Dao XS (2004) Wild vegetable resources and market survey in Xishuangbanna, Southwest China. Econ Bot 58:647–667

    Google Scholar 

  • Yan Z, Chen J, Li X (2013) Methyl jasmonate as modulator of Cd toxicity in Capsicum frutescens var. fasciculatum seedlings. Ecotoxicol Environ Saf 98:203–209

    CAS  Google Scholar 

  • Yang L, Huang S, Liu Y, Zheng S, Liu H, Rensing C, Fan Z, Feng R (2022) Selenate regulates the activity of cell wall enzymes to influence cell wall component concentration and thereby affects the uptake and translocation of Cd in the roots of Brassica rapa L. Sci Total Environ 821:153156

    CAS  Google Scholar 

  • Yu X, Zhang W, Zhang Y, Zhang X, Lang D, Zhang X (2018) The roles of methyl jasmonate to stress in plants. Funct Plant Biol 46:197–212

    Google Scholar 

  • Zhang S, Song J (2018) Geochemical cadmium anomaly and bioaccumulation of cadmium and lead by rapeseed (Brassica napus L.) from noncalcareous soils in the Guizhou Plateau. Sci Total Environ 644:624–634

    CAS  Google Scholar 

  • Zhang YP, Yang AM, Wang J, Zhang KK, Hu DY (2017) Assessment of cadmium content of potato grown in Weining County, Guizhou Province, Chin. Environ Monit Assess 189:226

    Google Scholar 

  • Zhu YG, Pilon-Smits EA, Zhao FJ, Williams PN, Meharg AA (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14:436–442

    CAS  Google Scholar 

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Chuhan Zhang: Data curation, Writing–original draft. Renquan Huang: Investigation, Data curation. Niheng Zhan: Data curation. Lijun Qin: Writing–review & editing.

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Correspondence to Lijun Qin.

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Zhang, C., Huang, R., Zhan, N. et al. Methyl jasmonate and selenium synergistically mitigative cadmium toxicity in hot pepper (Capsicum annuum L.) plants by improving antioxidase activities and reducing Cd accumulation. Environ Sci Pollut Res 30, 82458–82469 (2023). https://doi.org/10.1007/s11356-023-28273-7

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