24-Epibrassinolide mitigates nickel toxicity in young Eucalyptus urophylla S.T. Blake plants: nutritional, physiological, biochemical, anatomical and morphological responses

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Key message

Our research revealed that 24-epibrassinolide alleviated nickel toxicity in young Eucalyptus urophylla plants, inducing benefits on nutritional, physiological, biochemical, anatomical and morphological responses.


Soil contamination by heavy metals may limit the Eucalyptus production. Disturbances caused by nickel (Ni) toxicity interfere with the absorption of other essential nutrients. 24-Epibrassinolide (EBR) is one form of brassinosteroid (BR) that provides benefits for plant metabolism under Ni toxicity.


The aim of this study was to determine whether exogenous EBR can improve ionic homeostasis by evaluating nutrient concentrations, anatomical characteristics and chlorophyll fluorescence in young Eucalyptus urophylla plants subjected to Ni toxicity.


The experiment was randomized into four treatments, including two Ni concentrations (0 and 600 μM Ni) and two 24-epibrassinolide concentrations (0 and 100 nM EBR).


EBR significantly reduced Ni contents. Plants exposed to Ni2+ and sprayed with steroid had increases in the Ca2+/Ni2+ and Mn2+/Ni2+ ratios in the leaves of 38% and 15%, respectively, compared with the same treatment without EBR. The treatment of Ni2+ toxicity + EBR presented an increase of 42% in effective quantum yield of PSII photochemistry, when compared with plants exposed to Ni without EBR. Ni toxicity induced negative effects on stomatal functionality, but EBR application mitigated these effects.


Benefits on effective quantum yield of PSII photochemistry after EBR spray can be related to increases in manganese contents. EBR reduced oxidative stress, alleviating the deleterious effects induced by Ni toxicity and inducing positive repercussions on antioxidant enzymes, photosynthetic pigments and biomass.

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Fig. 1
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Fig. 6




C i :

Intercellular CO2 concentration

E :

Transpiration rate




Equatorial diameter of the stomata


Electrolyte leakage


Epidermis thickness from abaxial leaf side


Epidermis thickness from adaxial leaf side


Electron transport rate


Ratio between the apparent electron transport rate and net photosynthetic rate


Relative energy excess at the PSII level

F0 :

Minimal fluorescence yield of the dark-adapted state



Fm :

Maximal fluorescence yield of the dark-adapted state

Fv :

Variable fluorescence

Fv/Fm :

Maximal quantum yield of PSII photochemistry


Nonphotochemical quenching


Natural resistance-associated macrophage protein


Polar diameter of the stomata

P N :

Net photosynthetic rate

P N/C i :

Instantaneous carboxylation efficiency


Palisade parenchyma thickness

qP :

Photochemical quenching


Root cortex diameter


Root dry matter


Root metaxylem diameter


Root endodermis thickness


Root epidermis thickness


Stomatal density


Stem dry matter


Stomatal functionality


Stomatal index


Spongy parenchyma thickness


Total dry matter

Total Chl:

Total chlorophyll


Vascular cylinder diameter


Water-use efficiency


ZRT/IRT-like protein


Effective quantum yield of PSII photochemistry


  1. Adamski JM, Danieloski R, Deuner S, Braga EJB, Castro LAS, Peters JA (2012) Responses to excess iron in sweet potato: impacts on growth, enzyme activities, mineral concentrations, and anatomy. Acta Physiol Plant 34:1827–1836.

  2. Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013a) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213.

  3. Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013b) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213.

  4. Ahmad MSA, Hussain M, Saddiq R, Alvi AK (2007) Mungbean: a nickel indicator, accumulator or excluder? Bull Environ Contam Toxicol 78:319–324.

  5. Alam MM, Hayat S, Ali B, Ahmad A (2007) Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45:139–142.

  6. Ali B, Hayat S, Fariduddin Q, Ahmad A (2008) 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere 72:1387–1392.

  7. Ali E, Maodzeka A, Hussain N, Shamsi IH, Jiang L (2015) The alleviation of cadmium toxicity in oilseed rape (Brassica napus) by the application of salicylic acid. Plant Growth Regul 75:641–655.

  8. Amari T, Ghnaya T, Debez A, Taamali M, Ben Youssef N, Lucchini G, Sacchi GA, Abdelly C (2014) Comparative Ni tolerance and accumulation potentials between Mesembryanthemum crystallinum (halophyte) and Brassica juncea: metal accumulation, nutrient status and photosynthetic activity. J Plant Physiol 171:1634–1644.

  9. Andersson I, Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46:275–291.

  10. Aravind P, Prasad MNV (2004) Zinc protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte. Plant Sci 166:1321–1327.

  11. Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57.

  12. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93.

  13. Ashraf MY, Sadiq R, Hussain M, Ashraf M, Ahmad MS (2011) Toxic effect of nickel (Ni) on growth and metabolism in germinating seeds of sunflower (Helianthus annuus L.). Biol Trace Elem Res 143:1695–1703.

  14. Atabayeva S, Nurmahanova A, Akhmetova A et al (2016) Anatomical peculiarities in wheat (Triticum aestivum L.) varieties under copper stress. Pakistan J Bot 48:1399–1405

  15. Badawi GH, Yamauchi Y, Shimada E et al (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928.

  16. Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8.

  17. Bajguz A, Piotrowska-Niczyporuk A (2014) Interactive effect of brassinosteroids and cytokinins on growth, chlorophyll, monosaccharide and protein content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiol Biochem 80:176–183.

  18. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113.

  19. Bazihizina N, Redwan M, Taiti C et al (2015) Root based responses account for Psidium guajava survival at high nickel concentration. J Plant Physiol 174:137–146.

  20. Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. Int J Pure Appl Biosci 3:345–355.

  21. Bityutskii N, Pavlovic J, Yakkonen K et al (2014) Contrasting effect of silicon on iron, zinc and manganese status and accumulation of metal-mobilizing compounds in micronutrient-deficient cucumber. Plant Physiol Biochem 74:205–211.

  22. Bradford MM (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.

  23. Buonasera K, Lambreva M, Rea G, Touloupakis E, Giardi MT (2011) Technological applications of chlorophyll a fluorescence for the assessment of environmental pollutants. Anal Bioanal Chem 401:1139–1151.

  24. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468.

  25. Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227.

  26. Chen LS, Qi YP, Smith BR, Liu XH (2005) Aluminum-induced decrease in CO2 assimilation in citrus seedlings is unaccompanied by decreased activities of key enzymes involved in CO2 assimilation. Tree Physiol 25:317–324.

  27. Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. CLEAN - Soil, Air, Water 37:304–313.

  28. Choudhary SP, Yu J-Q, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Benefits of brassinosteroid crosstalk. Trends Plant Sci 17:594–605.

  29. Cristancho RJA, Hanafi MM, Omar SRS, Rafii MY (2014) Aluminum speciation of amended acid tropical soil and its effects on plant root growth. J Plant Nutr 37:811–827.

  30. Dallagnol LJ, Martins SCV, DaMatta FM, Rodrigues FÁ (2015) Brown spot negatively affects gas exchange and chlorophyll a fluorescence in rice leaves. Trop Plant Pathol 40:275–278.

  31. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228.

  32. Deng THB, Tang YT, van der Ent A et al (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45.

  33. Djebali W, Zarrouk M, Brouquisse R, el Kahoui S, Limam F, Ghorbel MH, Chaïbi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:358–368.

  34. Drążkiewicz M, Baszyński T (2010) Interference of nickel with the photosynthetic apparatus of Zea mays. Ecotoxicol Environ Saf 73:982–986.

  35. Dubey D, Pandey A (2011) Effect of nickel (Ni) on chlorophyll, lipid peroxidation and antioxidant enzymes activities in black gram (Vigna mungo) leaves. Int J Sci Nat 2:395–401

  36. Edel KH, Kudla J (2016) Integration of calcium and ABA signaling. Curr Opin Plant Biol 33:83–91.

  37. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620.

  38. Erb TJ, Zarzycki J (2018) A short history of RubisCO: the rise and fall (?) of nature’s predominant CO2 fixing enzyme. Curr Opin Biotechnol 49:100–107.

  39. Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9–17.

  40. Feng J, Shi Q, Wang X et al (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic (Amsterdam) 123:521–530.

  41. Gajewska E, Skłodowska M (2007) Relations between tocopherol, chlorophyll and lipid peroxides contents in shoots of Ni-treated wheat. J Plant Physiol 164:364–366.

  42. Gajewska E, Skłodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188.

  43. Galmés J, Flexas J, Savé R, Medrano H (2007) Water relations and stomatal characteristics of mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290:139–155.

  44. Gao J, Wang H, Yuan Q, Feng Y (2018) Structure and function of the photosystem supercomplexes. Front Plant Sci 9:1–7.

  45. Garcia JS, Dalmolin ÂC, Cortez PA, Barbeira PS, Mangabeira PAO, França MGC (2018) Short-term cadmium exposure induces gas exchanges, morphological and ultrastructural disturbances in mangrove Avicennia schaueriana young plants. Mar Pollut Bull 131:122–129.

  46. Ghassemi-Golezani K, Lotfi R (2015) The impact of salicylic acid and silicon on chlorophyll a fluorescence in mung bean under salt stress. Russ J Plant Physiol 62:611–616.

  47. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314

  48. Gomes MP, Marques TCLLSM, Carneiro MMLC, Soares ÂM (2012) Anatomical characteristics and nutrient uptake and distribution associated with the cd-phytoremediation capacity of Eucalyptus camaldulenses Dehnh. J Soil Sci Plant Nutr 12:481–495.

  49. Gong M, Li Y-J, Chen S-Z (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496.

  50. Gowayed SMH, Almaghrabi OA (2013) Effect of copper and cadmium on germination and anatomical structure of leaf and root seedling in maize ( Zea mays L). Aust J Basic Appl Sci 7:548–555

  51. Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537.

  52. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848.

  53. Harasim P, Filipek T (2015) Nickel in the environment. J Elem 20:525–534.

  54. Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455.

  55. Hayat S, Hasan SA, Yusuf M et al (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ Exp Bot 69:105–112.

  56. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908.

  57. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, 2nd edn. California Agricultural Experiment Station

  58. Hussain MB, Ali S, Azam A et al (2013) Morphological, physiological and biochemical responses of plants to nickel stress: a review. African J Agric Res 8:1596–1602.

  59. IBÁ (2017) Anuário Estatístico da Indústria Brasileira de Árvore - 2017. 100.

  60. Ibanes M, Fabregas N, Chory J, Cano-Delgado AI (2009) Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc Natl Acad Sci 106:13630–13635.

  61. Iori V, Pietrini F, Cheremisina A, Shevyakova NI, Radyukina N, Kuznetsov VV, Zacchini M (2013) Growth responses, metal accumulation and phytoremoval capability in amaranthus plants exposed to nickel under hydroponics. Water Air Soil Pollut 224:1–10.

  62. Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39.

  63. Jenbere D, Lemenih M, Kassa H (2012) Expansion of eucalypt farm forestry and its determinants in arsi negelle district, south Central Ethiopia. Small-scale For 11:389–405.

  64. Jesus LR, Batista BL, Lobato AKS (2017) Silicon reduces aluminum accumulation and mitigates toxic effects in cowpea plants. Acta Physiol Plant 39:138–114.

  65. Kanwar MK, Bhardwaj R, Chowdhary SP et al (2013) Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol Plant 35:1351–1362.

  66. Khaliq A, Ali S, Hameed A et al (2015) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis, and suppressing Ni uptake and oxidative stress. Arch Agron Soil Sci 62:633–647.

  67. Kočová M, Rothová O, Holá D, Kvasnica M, Kohout L (2010) The effects of brassinosteroids on photosynthetic parameters in leaves of two field-grown maize inbred lines and their F1 hybrid. Biol Plant 54:785–788.

  68. Korzeniowska J, Stanislawska-Glubiak E (2019) Phytoremediation potential of Phalaris arundinacea, Salix viminalis and Zea mays for nickel-contaminated soils. Int J Environ Sci Technol 16:1999–2008.

  69. Kumari J, Udawat P, Dubey AK, Haque MI, Rathore MS, Jha B (2017) Overexpression of SbSI-1, a nuclear protein from Salicornia brachiata confers drought and salt stress tolerance and maintains photosynthetic efficiency in transgenic tobacco. Front Plant Sci 8:1215.

  70. Kuramshina ZM, Smirnova YV, Khairullin RM (2018) Cadmium and nickel toxicity for Sinapis alba plants inoculated with endophytic strains of Bacillus subtilis. Russ J Plant Physiol 65:269–277.

  71. Laanemets K, Brandt B, Li J, Merilo E, Wang YF, Keshwani MM, Taylor SS, Kollist H, Schroeder JI (2013) Calcium-dependent and -independent stomatal signaling network and compensatory feedback control of stomatal opening via Ca2+ sensitivity priming. Plant Physiol 163:504–513.

  72. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570.

  73. Li S, Yang W, Yang T, Chen Y, Ni W (2015) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of elsholtzia argyi —a cadmium accumulating plant. Int J Phytoremediation 17:85–92.

  74. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Current protocols in food analytical chemistry. John Wiley & Sons, Inc., Hoboken, NJ, USA, pp 431–438

  75. Lima JV, Lobato AKS (2017) Brassinosteroids improve photosystem II efficiency, gas exchange, antioxidant enzymes and growth of cowpea plants exposed to water deficit. Physiol Mol Biol Plants 23:59–72.

  76. Lima MDR, Barros Junior UO, Batista BL, Lobato AKS (2018) Brassinosteroids mitigate iron deficiency improving nutritional status and photochemical efficiency in Eucalyptus urophylla plants. Trees - Struct Funct 32:1681–1694.

  77. Lukatkin AS, Kashtanova NN, Duchovskis P (2013) Changes in maize seedlings growth and membrane permeability under the effect of epibrassinolide and heavy metals. Russ Agric Sci 39:307–310.

  78. Maia CF, Silva BRS, Lobato AKS (2018) Brassinosteroids positively modulate growth: physiological, biochemical and anatomical evidence using two tomato genotypes contrasting to dwarfism. J Plant Growth Regul 37:1–14.

  79. Maksimović I, Kastori R, Krstić L, Luković J (2007) Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant 51:589–592.

  80. Maruthi Sridhar BB, Diehl SV, Han FX et al (2005) Anatomical changes due to uptake and accumulation of Zn and cd in Indian mustard (Brassica juncea). Environ Exp Bot 54:131–141.

  81. Matraszek R, Hawrylak-Nowak B, Chwil S, Chwil M (2016) Macronutrient composition of nickel-treated wheat under different sulfur concentrations in the nutrient solution. Environ Sci Pollut Res 23:5902–5914.

  82. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668.

  83. Mellor N, Adibi M, El-Showk S et al (2017) Theoretical approaches to understanding root vascular patterning: a consensus between recent models. J Exp Bot 68:5–16.

  84. Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+−transport abilities. Plant Physiol Biochem 43:793–801.

  85. Mora F, Arriagada O, Ballesta P, Ruiz E (2017) Genetic diversity and population structure of a drought-tolerant species of Eucalyptus, using microsatellite markers. J Plant Biochem Biotechnol 26:274–281.

  86. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216.

  87. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

  88. Neiva D, Fernandes L, Araújo S et al (2015) Chemical composition and Kraft pulping potential of 12 eucalypt species. Ind Crop Prod 66:89–95.

  89. Nie J, Pan Y, Shi J, Guo Y, Yan Z, Duan X, Xu M (2015) A comparative study on the uptake and toxicity of nickel added in the form of different salts to maize seedlings. Int J Environ Res Public Health 12:15075–15087.

  90. Nishida S, Tsuzuki C, Kato A et al (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442.

  91. O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

  92. Ortega L, Fry SC, Taleisnik E (2006) Why are Chloris gayana leaves shorter in salt-affected plants? Analyses in the elongation zone. J Exp Bot 57:3945–3952.

  93. Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758.

  94. Parry MAJ, Andralojc PJ, Scales JC et al (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64:717–730.

  95. Pérez Chaca MV, Vigliocco A, Reinoso H, Molina A, Abdala G, Zirulnik F, Pedranzani H (2014) Effects of cadmium stress on growth, anatomy and hormone contents in Glycine max (L.) Merr. Acta Physiol Plant 36:2815–2826.

  96. Pietrini F, Iori V, Cheremisina A, Shevyakova NI, Radyukina N, Kuznetsov VV, Zacchini M (2015) Evaluation of nickel tolerance in Amaranthus paniculatus L. plants by measuring photosynthesis, oxidative status, antioxidative response and metal-binding molecule content. Environ Sci Pollut Res 22:482–494.

  97. Poorter H, Niinemets Ü, Poorter L et al (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588.

  98. Qin L, Kang W, Qi Y et al (2016) The influence of silicon application on growth and photosynthesis response of salt stressed grapevines (Vitis vinifera L.). Acta Physiol Plant 38:68.

  99. Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:1–5.

  100. Reeves RD, Baker AJM, Becquer T et al (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293:107–119.

  101. Rehman MZ, Rizwan M, Ali S et al (2016) Contrasting effects of biochar, compost and farm manure on alleviation of nickel toxicity in maize (Zea mays L.) in relation to plant growth, photosynthesis and metal uptake. Ecotoxicol Environ Saf 133:218–225.

  102. Ribeiro MAQ, Almeida A-AF, Mielke MS et al (2013) Aluminum effects on growth, photosynthesis, and mineral nutrition of cacao genotypes. J Plant Nutr 36:1161–1179.

  103. Ribeiro AT, Oliveira VP, Barros Junior UO, Silva BRS, Batista BL, Lobato AKS (2019) Data linked to publication entitled 24-Epibrassinolide mitigates nickel toxicity in young Eucalyptus urophylla S.T. Blake plants: nutritional, physiological, biochemical, anatomical and morphological responses. V2. Zenodo. [dataset].

  104. Rio LA, Corpas FJ, Sandalio L et al (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81.

  105. Rouached H, Secco D, Arpat BA (2010) Regulation of ion homeostasis in plants: current approaches and future challenges. Plant Signal Behav 5:501–502.

  106. Saad R, Kobaissi A, Robin C et al (2016) Nitrogen fixation and growth of Lens culinaris as affected by nickel availability: a pre-requisite for optimization of agromining. Environ Exp Bot 131:1–9.

  107. Sagardoy R, Vázquez S, Florez-Sarasa ID, Albacete A, Ribas-Carbó M, Flexas J, Abadía J, Morales F (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol 187:145–158.

  108. Santos EF, Santini JMK, Paixão AP et al (2017) Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol Biochem 113:6–19.

  109. Santos LR, Batista BL, Lobato AKS (2018) Brassinosteroids mitigate cadmium toxicity in cowpea plants. Photosynthetica 56:591–605.

  110. Schmidt SB, Jensen PE, Husted S (2016) Manganese deficiency in plants: the impact on photosystem II. Trends Plant Sci 21:622–632.

  111. Segatto FB, Bisognin DA, Benedetti M et al (2004) A technique for the anatomical study of potato leaf epidermis. Ciência Rural 34:1597–1601.

  112. Seldimirova OA, Bezrukova MV, Galin IR, Lubyanova AR, Shakirova FM, Kruglova NN (2017) 24-epibrassinolide effects on in vitro callus tissue formation, growth, and regeneration in wheat varieties with contrasting drought resistance. Russ J Plant Physiol 64:919–929.

  113. Sellami R, Gharbi F, Rejeb S, Rejeb MN, Henchi B, Echevarria G, Morel JL (2012) Effects of nickel hyperaccumulation on physiological characteristics of alyssum Murale grown on metal contaminated waste amended soil. Int J Phytoremediation 14:609–620.

  114. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277.

  115. Sharma A, Dhiman A (2013) Nickel and cadmium toxicity in plants. J Pharm Sci Innov 2:20–24.

  116. Sharma I, Pati PK, Bhardwaj R (2011) Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 33:1723–1735.

  117. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26.

  118. Sharma A, Thakur S, Kumar V, Kesavan AK, Thukral AK, Bhardwaj R (2017) 24-epibrassinolide stimulates imidacloprid detoxification by modulating the gene expression of Brassica juncea L. BMC Plant Biol 17:1–10.

  119. Shutilova NI (2010) The oxygen-evolving complex of chloroplast membranes. Biochem Suppl Ser A Membr Cell Biol 4:125–133.

  120. Siddiqui H, Hayat S, Bajguz A (2018) Regulation of photosynthesis by brassinosteroids in plants. Acta Physiol Plant 40:1–15.

  121. Silva EN, Ribeiro RV, Ferreira-Silva SL et al (2012) Coordinate changes in photosynthesis, sugar accumulation and antioxidative enzymes improve the performance of Jatropha curcas plants under drought stress. Biomass Bioenergy 45:270–279.

  122. Sirhindi G, Mir MA, Abd-Allah EF et al (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Front Plant Sci 7:1–12.

  123. Soares C, de Sousa A, Pinto A et al (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125.

  124. Sorin C, Musse M, Mariette F, Bouchereau A, Leport L (2015) Assessment of nutrient remobilization through structural changes of palisade and spongy parenchyma in oilseed rape leaves during senescence. Planta 241:333–346.

  125. Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140.

  126. Steel RG, Torrie JH, Dickey DA (2006) Principles and procedures of statistics: a biometrical approach, 3rd edn. Academic Internet Publishers, Moorpark

  127. Tadele D, Teketay D (2014) Growth and yield of two grain crops on sites former covered with eucalypt plantations in Koga watershed, northwestern Ethiopia. J For Res 25:935–940.

  128. Vázquez MN, Guerrero YR, González LM, Noval WT (2013) Brassinosteroids and plant responses to heavy metal stress. An overview. Open J Met 3:34–41.

  129. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants protective role of exogenous polyamines. Plant Sci 151:59–66.

  130. Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066.

  131. Wu Q-S, Xia R-X, Zou Y-N (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110.

  132. Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2011a) Protective response of 28-homobrassinolide in cultivars of triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60:68–76.

  133. Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011b) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17.

  134. Yusuf M, Fariduddin Q, Ahmad A (2012) 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiata under different levels of nickel: a shotgun approach. Plant Physiol Biochem 57:143–153.

  135. Yusuf M, Fariduddin Q, Ahmad I, Ahmad A (2014) Brassinosteroid-mediated evaluation of antioxidant system and nitrogen metabolism in two contrasting cultivars of Vigna radiata under different levels of nickel. Physiol Mol Biol Plants 20:449–460.

  136. Zhou YM, Han SJ (2005) Photosynthetic response and stomatal behaviour of Pinus koraiensis during the fourth year of exposure to elevated CO2 concentration. Photosynthetica 43:445–449.

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Correspondence to Allan Klynger da Silva Lobato.

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Ribeiro, A.T., de Oliveira, V.P., de Oliveira Barros Junior, U. et al. 24-Epibrassinolide mitigates nickel toxicity in young Eucalyptus urophylla S.T. Blake plants: nutritional, physiological, biochemical, anatomical and morphological responses. Annals of Forest Science 77, 5 (2020) doi:10.1007/s13595-019-0909-9

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  • Eucalyptus urophylla
  • Light capture
  • Metal contamination
  • Nutritional balance
  • 24-epibrassinolide