Skip to main content
SpringerLink
Log in

Exogenous application of jasmonates and brassinosteroids alleviates lead toxicity in bamboo by altering biochemical and physiological attributes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Exogenous application of phytohormones is getting promising results in alleviating abiotic stresses, particularly heavy metal (HMs). Jasmonate (JA) and brassinosteroid (BR) have crosstalk in bamboo plants, reflecting a burgeoning area of investigation. Lead (Pb) is the most common pollutant in the environment, adversely affecting plants and human health. The current study focused on the foliar application of 10 µM JA and 10 µM BR in both single and combination forms on bamboo plants grown under Pb stress (0, 50, 100, 150 µM) with a completely randomized design by four replications. The study found that applying 10 µM JA and 10 µM BR significantly improves growth and tolerance by reducing oxidative stress, reactive oxygen species including hydrogen peroxide (H2O2, 32.91%), superoxide radicals (O2−•, 33.9%), methylglyoxal (MG, 19%), membrane lipoperoxidation (25.66%), and electrolyte leakage (41.5%) while increasing antioxidant (SOD (18%), POD (13%), CAT (20%), APX (12%), and GR (19%)), non-antioxidant (total phenolics (7%), flavonols (12.3%), and tocopherols (13.8%)), and glyoxylate activity (GLyI (13%), GLyII (19%)), proline content (19%), plant metal chelating capacity (17.3%), photosynthetic pigments (16%), plant growth (10%), and biomass (12%). We found that JA and BR, in concert, boost bamboo species’ Pb tolerance by enhancing antioxidant and glyoxalase cycles, ion chelation, and reducing metal translocation and accumulation. This conclusively demonstrates that utilizing a BR–JA combination form at 10 µM dose may have the potential to yield optimal efficiency in mitigating oxidative stress in bamboo plants.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Data will be made available on request from the corresponding author.

References

  • Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462

    CAS  Google Scholar 

  • Aebi H (1984) “Catalase in vitro”. In: Methods in enzymology, vol. 105, Elsevier, 121–126

  • Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Guce S (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813

    Google Scholar 

  • Ahmad P, Alyemeni M, Vijaya L, Alam P, Abass M, Alamri S (2017) Jasmonic acid alleviates negative impacts of cadmium stress by modifying osmolytes and antioxidants in faba bean (Vicia faba L.). Arch Agron Soil Sci 63:1889

    CAS  Google Scholar 

  • Ahmad Z, Upadhyay A, Ding YL, Emamverdian A, Shahzad A (2021) Bamboo: origin, habitat, distributions and global prospective. In: Ahmad Z, Ding Y, Shahzad A (eds) Biotechnological Advances in Bamboo. Springer, Singapore, pp 1–31

    Google Scholar 

  • Akkol EK, Goger F, Koşar M, Başer KHC (2008) Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chem 108:942–949

    CAS  Google Scholar 

  • Ali E, Hussain N, Shamsi IH, Jabeen Z, Siddiqui MH, Jiang LX (2008) Role of jasmonic acid in improving tolerance of rapeseed (Brassica napus L.) to Cd toxicity. J Zhejiang Univ Sci B 19(2):130–146. https://doi.org/10.1631/jzus.B1700191

    Article  Google Scholar 

  • Ali B, Hasan SA, Hayat S, Hayat Q, Yadav S, Fariduddin QA (2008) Role for brassinosteroids in the amelioration of aluminum stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ Exp Bot 62:153

    CAS  Google Scholar 

  • Aneczko A, Koscielniak J, Pilipowicz M, Szarek-lukaszewska G, Skoczowski A (2005) Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. Photosynthetica 43:293

    Google Scholar 

  • Bajguz A (2000) Blockade of heavy metals accumulation in Chlorella vulgaris cells by 24-epibrassinolide. Plant Physiol Biochem 38:797–801. https://doi.org/10.1016/S0981-9428(00)01185-2

    Article  CAS  Google Scholar 

  • Bajguz A (2002) Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 159:321

    CAS  Google Scholar 

  • Bal LM, Singhal P, Satya S, Naik SN, Kar A (2012) Bamboo shoot preservation for enhancing its business potential and local economy: a review. J Crit Rev Food Sci Nutr 52:804–814

    Google Scholar 

  • Bali S, Kaur P, Kohli SK, Ohri P, Thukral AK, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2018) Jasmonic acid induced changes in physio-biochemical attributes and ascorbate-glutathione pathway in Lycopersicon esculentum under lead stress at different growth stages. Sci Total Environ 645:1344–1360

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060

    Article  CAS  Google Scholar 

  • Bedabati Chanu L, Gupta A (2016) Phytoremediation of lead using Ipomoea aquatica Forsk. in hydroponic solution. Chemosphere 156:407–411

    CAS  Google Scholar 

  • Bhardwaj R, Sharma I, Kapoor D, Vandana P, Gautam V, Kaur R, Bali S, Sharma A (2014) Brassinosteroids: improving crop productivity and abiotic stress tolerance. In: Ahmad P, Wani M (eds) Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, NY

    Google Scholar 

  • Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9):e04691. https://doi.org/10.1016/j.heliyon.2020.e04691

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

    CAS  Google Scholar 

  • Chen R, Sherbinin AD, Ye C, Shi G (2014b) China’s soil pollution: farms on the frontline. Science 344(6185):691

    CAS  Google Scholar 

  • Chen Z, Gao X, Zhang J, Bonfante P, Genre A, Al-Babili S (2015) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 6:209

    Google Scholar 

  • Chew Y-L, Goh J-K, Lim Y-Y (2009) Assessment of in-vitro antioxidant capacity and polyphenolic composition of selected medicinal herbs from Leguminosae family in Peninsular Malaysia. Food Chem 116:13–18

    CAS  Google Scholar 

  • Choudhary SP, Volkan Oral H, Bhardwaj R, Yu JQ (2012) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63(15):5659

    CAS  Google Scholar 

  • Dao LHD, Beardall J (2016) Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Res 16:150–159

    Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053

  • Daszkowska-Golec A, Szarejko I (2013) Open or close the gate—stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138

    Google Scholar 

  • De Vos CH, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98(3):853–858. https://doi.org/10.1104/pp.98.3.853

    Article  Google Scholar 

  • Dhar N, Gopalan N, Nikhil P, Mohapatra S (2022) Role of phytohormones in plant-microbial interaction auxins, cytokinins and gibberellins signaling in plants. Springer 313–336

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91. https://doi.org/10.1093/jxb/32.1.79

    Article  CAS  Google Scholar 

  • Dikilitas M, Karakas S, Ahmad P (2016) Effect of lead on plant and human DNA damages and its impact on the environment. Plant Metal Interact

  • Doganlar ZB (2012) Physiological and genetic responses to pesticide mixture treatment of Veronica beccabunga. Water Air Soil Pollut 223:6201

    CAS  Google Scholar 

  • Emamverdian A, Ding Y (2017) Effects of heavy metals’ toxicity on plants and enhancement of plant defense mechanisms of Si-mediation “Review.” Int J Environ Agric Res 3(4):41–51

    Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2018a) Growth responses and photosynthetic indices of bamboo plant (Indocalamus latifolius) under heavy metal stress. Sci World J 2018:1219364

    Google Scholar 

  • Emamverdian Y, Ding Y, Xie Y (2018b) Phytoremediation potential of bamboo plant in China. Ecol Environ Conserv 24:530–539

    Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F et al (2020a) Silicon dioxide nanoparticles improve plant growth by enhancing antioxidant enzyme capacity in bamboo (Pleioblastus pygmaeus) under lead toxicity. Trees 34:469–481. https://doi.org/10.1007/s00468-019-01929-z

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Xie Y (2020b) The role of new members of phytohormones in plant amelioration under abiotic stress with an emphasis on heavy metals. Pol J Environ 29:1009–1020

    CAS  Google Scholar 

  • Emamverdian A, Ding Y, Ranaei F, Ahmad Z (2020c) Application of bamboo plants in nine aspects. Sci World J 2020:7284203. https://doi.org/10.1155/2020/7284

    Article  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Ahmad Z (2021) Mechanisms of selected plant hormones under heavy metal stress. Pol J Environ Stud 30:497–507

    CAS  Google Scholar 

  • Emamverdian A, Ding Y, Barker J, Liu G, Li Y, Mokhberdoran F (2023a) Sodium nitroprusside improves bamboo resistance under Mn and Cr toxicity with stimulation of antioxidants activity, relative water content, and metal translocation and accumulation. Int J Mol Sci 24:1942. https://doi.org/10.3390/ijms24031942

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Hasanuzzaman M, Barker J, Liu G, Li Y, Mokhberdoran F (2023b) Insight into the biochemical and physiological mechanisms of nanoparticles-induced arsenic tolerance in bamboo. Front Plant Sci 14:1121886. https://doi.org/10.3389/fpls.2023.1121886

    Article  Google Scholar 

  • Emamverdian A, Ghorbani A, Li Y, Pehlivan N, Barker J, Ding Y, Liu G, Zargar M (2023c) Responsible mechanisms for the restriction of heavy metal toxicity in plants via the co-foliar spraying of nanoparticles. Agronomy 13(7):1748

    CAS  Google Scholar 

  • Emamverdian A, Ghorbani A, Pehlivan N, Alwahibi MS, Elshikh MS, Liu G, ... Chen M (2023d) Co-application of melatonin and zeolite boost bamboo tolerance under cadmium by enhancing antioxidant capacity, osmolyte accumulation, plant nutrient availability, and decreasing cadmium absorption. Sci Hortic 322:112433

  • Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9

    CAS  Google Scholar 

  • Felisberto MHF, Miyake PSE, Beraldo AL, Clerici MTPS (2017) Young bamboo culm: potential food as source of fiber and starch. Food Res Int 101:96–102

    CAS  Google Scholar 

  • Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 66(3):482–487. https://doi.org/10.1104/pp.66.3.482

    Article  CAS  Google Scholar 

  • Gupta S, Kumar D, Gaur JP (2009) Kinetic and isotherm modeling of lead(II) sorption onto some waste plant materials. Chem Eng J 148:226

    CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum l.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22(3):584–596

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011a) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353. https://doi.org/10.1007/s11816-011-018

    Article  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011b) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143(3):1704–1721

    CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M et al (2017) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18(1):200

    Google Scholar 

  • Hayat S, Alyemeni MN, Hasan SA (2012) Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J Biol Sci 19:325

    CAS  Google Scholar 

  • He M, Ren T, Jin ZD, Deng L, Liu H, Cheng YY,... Chang H (2023) Precise analysis of potassium isotopic composition in plant materials by multi-collector inductively coupled plasma mass spectrometry. Spectrochim Acta Part B: At Spectrosc 106781. https://doi.org/10.1016/j.sab.2023.106781

  • Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiol 156:430

    CAS  Google Scholar 

  • Huang YP, Hou CH, His HC, Wu JW (2015) Optimization of highly microporous activated carbon preparation from Moso bamboo using central composite design approach. J Taiwan Inst Chem Eng 50:266–275

    CAS  Google Scholar 

  • Huang Z, Jin SH, Guo HD, Zhong XJ, He J, Li X, Jiang MY, Yu XF, Long H, Ma MD, Che QB (2016a) Genome-wide identification and characterization of TIFY family genes in Moso Bamboo (Phyllostachys edulis) and expression profiling analysis under dehydration and cold stresses. Peer J 4:e2620

    Google Scholar 

  • Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance regulation of proline metabolism. Environ Exp Bot 100:34

    CAS  Google Scholar 

  • Jin QY, Peng HZ, Lin EP, Li N, Huang DN, Xu YL, Hua XQ, Wang KH, Zhu TJ (2016) Identification and characterization of differentially expressed miRNAs between bamboo shoot and rhizome shoot. J Plant Biol 59:322–335

    CAS  Google Scholar 

  • Jung C, Maeder V, Funk F, Frey B, Sticher H, Frossard E (2003) Release of phenols from Lupinus albus L. roots exposed to Cu and their possible role in Cu detoxification. Plant Soil 252:301–312

    CAS  Google Scholar 

  • Kang DJ, Seo YJ, Lee JD, Ishii R, Kim KU, Shin DH (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars. J Agron Crop Sci 191:273

    CAS  Google Scholar 

  • Kanwar MK, Bhardwaj R, Arora P, Chowdhary SP, Sharma P, Kumar S (2012) Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica juncea L. Chemosphere 86:41

    CAS  Google Scholar 

  • Kayden HJ, Chow CK, Bjornson LK (1973) Spectrophotometric method for determination of tocopherol in red blood cells. J Lipid Res 14:533–540

    CAS  Google Scholar 

  • Keramat B, Kalantari KM, Arvin MJ (2009) Effects of methyl jasmonate in regulating cadmium induced oxidative stress in soybean plant (Glycine max L.). Afr J Microbiol Res 3:240

    CAS  Google Scholar 

  • Koeduka T, Matsui K, Hasegawa M, Akakabea Y, Kajiwara T (2005) Rice fatty acid-dioxygenase is induced by pathogen attack and heavy metal stress: activation through jasmonate signaling. J Plant Physiol 162:912

    CAS  Google Scholar 

  • Kour J, Kohli SK, Khanna K, Bakshi P, Sharma P, Singh AD, Ibrahim M, Devi K, Sharma N, Ohri P, Skalicky M, Brestic M, Bhardwaj R, Landi M, Sharma A (2021) Brassinosteroid signaling, crosstalk and physiological functions in plants under heavy metal stress. Front Plant Sci 12:608061. https://doi.org/10.3389/fpls.2021.608061

    Article  Google Scholar 

  • Kováčik J, Klejdus B, Štork F, Hedbavny J, Bačkor M (2011) Comparison of methyl jasmonate and cadmium effect on selected physiological parameters in Scenedesmus quadricauda (Chlorophyta, Chlorophyceae). J Phycol 47:1044

    Google Scholar 

  • Krzesłowska M, Rabęda I, Basińska A, Lewandowski M, Mellerowicz EJ, Napieralska A, Samardakiewicz S, Woźny A (2016) Pectinous cell wall thickenings formation – a common defense strategy of plants to cope with Pb. Environ Pollut 214:354–361

    Google Scholar 

  • Li C, Bai T, Ma F, Han M (2010) Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species. Sci Hortic 124:274–279. https://doi.org/10.1016/j.scienta.2009.12.029

    Article  CAS  Google Scholar 

  • Li J, Huang Y, Hu Y, Jin S, Bao Q, Wang F, Xiang M, Xie X (2016) Lead toxicity thresholds in 17 Chinese soils based on substrate-induced nitrification assay. J Environ Sci (china) 44:131–140

    Google Scholar 

  • Li Y, Mo X, Xiong J, Huang K, Zheng M, Jiang Q, Jiang C (2023) Deciphering the probiotic properties and safety assessment of a novel multi-stress-tolerant aromatic yeast Pichia kudriavzevii HJ2 from marine mangroves. Food Biosci 56:103248. https://doi.org/10.1016/j.fbio.2023.103248

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. In: Wrolstad RE, Acree TE, An H, Decker EA, Penner MH, Reid DS et al (eds) Current protocols in food analytical chemistry. John Wiley & Sons, Inc, Hoboken, NJ, USA, p 4

    Google Scholar 

  • Lu L, Zhai X, Li X, Wang S, Zhang L, Wang L, Wang F (2022) Met1-specific motifs conserved in OTUB subfamily of green plants enable rice OTUB1 to hydrolyze Met1 ubiquitin chains. Nat Commun 13(1):4672. https://doi.org/10.1038/s41467-022-32364-3

    Article  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21

    CAS  Google Scholar 

  • Lyer S, Sengupta C, Velumani A (2015) Lead toxicity: an overview of prevalence in Indians. Clin Chim Acta 451:161–164

    Google Scholar 

  • Maksymiec W, Krupa Z (2002) Jasmonic acid and heavy metals in Arabidopsis plants – a similar physiological response to both stressors? J Plant Physiol 159:509

    CAS  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Stud 15(523–530):61

    Google Scholar 

  • Mir MA, John R, Alyemeni MN, Alam P, Ahmad P (2018) Jasmonic acid ameliorates alkaline stress by improving growth performance, ascorbate glutathione cycle and glyoxylase system in maize seedlings. Sci Rep 8:2831

    Google Scholar 

  • Murashige T, Skoog FA (1962) Revised medium for rapid growth andbio assays with tobacco tissue cultures. Physiol Plant 15:73–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nie S, Mo S, Gao T, Yan B, Shen P, Kashif M, Jiang C (2023) Coupling effects of nitrate reduction and sulfur oxidation in a subtropical marine mangrove ecosystem with Spartina alterniflora invasion. Sci Total Environ 862:160930. https://doi.org/10.1016/j.scitotenv.2022.160930

    Article  CAS  Google Scholar 

  • Nováková O, Kuneš I, Gallo J, Baláš M (2014) Effects of brassinosteroids on prosperity of Scots pine seedlings. J for Sci 60(9):388

    Google Scholar 

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492. https://doi.org/10.1016/0003-2697(84)90039-3

    Article  CAS  Google Scholar 

  • Pehlivan N, Wang JJ (2022) Transcriptional insights into Cu related tolerance strategies in maize linked to a novel tea-biochar. Env Pol 293:118500

    CAS  Google Scholar 

  • Pehlivan N, Gedik K, Wang JJ (2023) Tea-based biochar-mediated changes in cation diffusion homeostasis in rice grown in heavy metal (loid) contaminated mining soil. Plant Physiol Biochem 201:107889

    CAS  Google Scholar 

  • Peng Z, Han C, Yuan L, Zhang K, Huang H, Ren C (2011) Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. J Integr Plant Bio 53:632–640. https://doi.org/10.1111/j.1744-7909.2011.01042.x

    Article  CAS  Google Scholar 

  • Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J (2009) The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell Biol 41(8–9):1665–77

    CAS  Google Scholar 

  • Piotrowska A, Bajguz A, Godlewska-żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507

    CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136. https://doi.org/10.1007/978-1-4419-9860-6_4

    Article  CAS  Google Scholar 

  • Principato GB, Rosi G, Talesa V, Giovannini E, Uotila L (1987) Purification and characterization of two forms of glyoxalase II from the liver and brain of Wistar rats. Biochim Biophys Acta 911(3):349–355

    CAS  Google Scholar 

  • Qin X, Kaiduan Z, Fan Y, Fang H, Yong N,... Wu X (2022) The bacterial MtrAB two-component system regulates the cell wall homeostasis responding to environmental alkaline stress. Microbiol Spectr 10(5). https://doi.org/10.1128/spectrum.02311-22

  • Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:629

    Google Scholar 

  • Ramakrishna B, Rao SS (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252:665

    CAS  Google Scholar 

  • Repkina N, Murzina SA, Voronin VP, Kaznina N (2023) Does methyl jasmonate effectively protect plants under heavy metal contamination? Fatty acid content in wheat leaves exposed to cadmium with or without exogenous methyl jasmonate application. Biomolecules 13:582. https://doi.org/10.3390/biom13040582

    Article  CAS  Google Scholar 

  • Salazar MJ, Rodriguez JH, Cid CV, Pignata ML (2016) Auxin effects on Pb phytoextraction from polluted soils by Tegetes minuta L and Bidens pilosa L: extractive power of their root exudates. J Hazard Mater 5(311):63–9

    Google Scholar 

  • Schäfer M, Brütting C, Meza-Canales ID, Großkinsky DK, Vankova R, Baldwin IT, Meldau S (2015) The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J Exp Bot 66:4873–4884

    Google Scholar 

  • Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard Mater 325:36–58

    CAS  Google Scholar 

  • Sharma P, Bhardwaj R, Arora N, Arorah K (2007) Effect of 28-homobrassinolide on growth, zinc metal uptake and antioxidative enzyme activities in Brassica juncea L. seedlings. Braz J Plant Physiol 19:203

    CAS  Google Scholar 

  • Sharma P, Kaur H, Sirhindi G (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Millsp. seedlings under copper stress. Am J Plant Sci 04 (04)

  • Sharma I, Sharma A, Pati P, Bhardwaj R (2018) Brassinosteroids reciprocates heavy metals induced oxidative stress in radish by regulating the expression of key antioxidant enzyme genes. Braz Arch Biol Technol 61

  • Siddique YH, Ara G, Afzal M (2012) Estimation of lipid peroxidation induced by hydrogen peroxide in cultured human lymphocytes. Dose Response 10(1):1–10. https://doi.org/10.2203/dose-response.10-002.Siddique

    Article  CAS  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 8(6):1143. https://doi.org/10.3389/fpls.2015.01143.PMID:26904030;PMCID:PMC4744854

    Article  Google Scholar 

  • Sohn SI, Pandian S, Rakkammal K, Largia MJV, Thamilarasan SK, Balaji S, Zoclanclounon YAB, Shilpha J, Ramesh M (2022) Jasmonates in plant growth and development and elicitation of secondary metabolites: an updated overview. Front Plant Sci 15(13):942789. https://doi.org/10.3389/fpls.2022.942789

    Article  Google Scholar 

  • Souri Z, Karimi N (2017) Enhanced phytoextraction by As hyperaccumulator Isatis cappadocica spiked with sodium nitroprusside. Soil Sediment Contam 26:457–468

    CAS  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzalka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999. https://doi.org/10.1007/s11738-012-1169-6

    Article  CAS  Google Scholar 

  • Tang Y, Yang G, Liu X, Qin L, Zhai W, Fodjo EK, Kong C (2023) Rapid sample enrichment, novel derivatization, and high sensitivity for determination of 3-chloropropane-1,2-diol in soy sauce via high-performance liquid chromatography–tandem mass spectrometry. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.3c05230

    Article  Google Scholar 

  • Valentovic P, Luxova M, Kolarovic L, Gasparikova O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ. 52:184. https://doi.org/10.17221/3364-PSE

    Article  Google Scholar 

  • Verslues PE (2016) ABA and cytokinins: challenge and opportunity for plant stress research. Plant Mol Biol 91(6):629

    CAS  Google Scholar 

  • Vob U, Bishopp A, Farcot E, Bennett MJ (2014) Modelling hormonal response and development. Trends Plant Sci 19:311

    Google Scholar 

  • Wang P, Xu X, Tang Z, Zhang W, Huang XY, Zhao FJ (2018) OsWRKY28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice. Front Plant Sci 9:1330. https://doi.org/10.3389/fpls.2018.01330

    Article  CAS  Google Scholar 

  • Wani SG, Kumar V, Shriram V, Kumarsah S (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162

    Google Scholar 

  • Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Molecular Plant 9(1):86

    CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579(27):6265–6271

    CAS  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

    CAS  Google Scholar 

  • Yan Z, Zhang W, Chen J et al (2015) Methyl jasmonate alleviates cadmium toxicity in Solanum nigrum by regulating metal uptake and antioxidative capacity. Biol Plant 59:373–381. https://doi.org/10.1007/s10535-015-0491-4

    Article  CAS  Google Scholar 

  • Yu MH, Zhao ZZ, He JX (2018) Brassinosteroid signaling in plant-microbe interactions. Int J Mol Sci 19(12):4091

    Google Scholar 

  • Yusuf M, Fariduddin Q, Ahmad A (2011) 28-Homobrassinolide mitigates boron induced toxicity through enhanced antioxidant system in Vigna radiata plants. Chemosphere 85:1574

    CAS  Google Scholar 

  • Zhang X, Zhong T, Liu L, Ouyang X (2015) Impact of soil heavy metal pollution on food safety in China. PLoS One 10:e0135182

    Google Scholar 

  • Zhang X (1992) The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. Res. Method. Crop Physiol. X.Z. Zhang, ed., Beijing: Agriculture Press, 208–211

  • Zhao FJ, Ma Y, Zhu YJ, Tang Z, McGrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750–759

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Peijian Shi, Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, Jiangsu, China, for helping in the statistical analysis of the manuscript. This work was supported by RUDN University Strategic Academic Leadership Program.

Funding

The authors extend their appreciation to the Deanship of the Scientific Research at King Khalid University for funding this work through large group Research Project under grant number RGP2/280/44.

Author information

Authors and Affiliations

  1. Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, 210037, China

    Abolghassem Emamverdian

  2. Bamboo Research Institute, Nanjing Forestry University, Nanjing, 210037, China

    Abolghassem Emamverdian

  3. Biology Department, Faculty of Science, King Khalid University, P.O. Box 9004, 61413, Abha, Saudi Arabia

    Ahlam Khalofah

  4. Research Center for Advanced Materials Science (RCAMS), King Khalid University, P.O. Box 9004, 61413, Abha, Saudi Arabia

    Ahlam Khalofah

  5. Department of Biology, Recep Tayyip Erdogan University, Rize, 53100, Türkiye

    Necla Pehlivan

  6. Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, 38000, Punjab, Pakistan

    Muhammad Zia-ur-Rehman

  7. Department of Mathematical Sciences, Florida Atlantic University, Boca Raton, FL, 33431, USA

    Yang Li

  8. Department of Agrobiotechnology, Institute of Agriculture, RUDN University, 117198, Moscow, Russia

    Meisam Zargar

Authors
  1. Abolghassem Emamverdian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahlam Khalofah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Necla Pehlivan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Zia-ur-Rehman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meisam Zargar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AE: conceptualization, formal analysis, investigation, resources, data curation, writing—original draft, writing—review and editing, visualization, project administration. AK: conceptualization, resources, validation, data curation, visualization, supervision, writing—original draft, writing—review and editing. NP: methodology, formal analysis, data curation, writing—original draft, writing—review and editing. MZ-u-R: conceptualization, resources, writing—original draft, writing—review and editing, project administration. YL: methodology, formal analysis, data curation. MZ: conceptualization, writing—original draft, writing—review and editing.

Corresponding author

Correspondence to Abolghassem Emamverdian.

Ethics declarations

Consent to participate

All authors agreed to contribute to this study.

Conflict of interest

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.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Emamverdian, A., Khalofah, A., Pehlivan, N. et al. Exogenous application of jasmonates and brassinosteroids alleviates lead toxicity in bamboo by altering biochemical and physiological attributes. Environ Sci Pollut Res 31, 7008–7026 (2024). https://doi.org/10.1007/s11356-023-31549-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-31549-7

Keywords

Search

Navigation