Abstract
The aim of this research was to determine whether 24-epibrassinolide can mitigate oxidative stress in soybean plants subjected to different zinc levels; to examine this, we evaluated the possible repercussions on anatomical, nutritional, biochemical, physiological and morphological behaviours. The experiment followed a completely randomized factorial design with two concentrations of 24-epibrassinolide (0 and 100 nM EBR, described as - EBR and + EBR, respectively) and three zinc supplies (0.2, 20 and 2000 μM Zn, described as low, control and a high supply of Zn). In general, low and high zinc supplies produced deleterious effects. However, plants exposed to high zinc +100 nM EBR presented increases of 25%, 7%, 9% 29% and 69% for root epidermis, root endodermis, root cortex, vascular cylinder and metaxylem, respectively, when compared to the same treatment without the steroid. The steroid spray alleviated the impact produced by zinc stress on nutritional status, and these results were intrinsically linked to incremental changes in root structure, mainly vascular cylinder and metaxylem. Antioxidant enzymes play crucial roles in the photosynthetic machinery of plants treated with 24-epibrassinolide and stressed by high and low zinc supply, modulating reactive oxygen species scavenging and protecting the chloroplast membranes, with clear positive repercussions on photosystem II efficiency and photosynthetic pigments. The stimulation induced by this steroid on gas exchange can be explained by the favourable conditions detected in stomatal performance and leaf anatomy, thus enhancing the diffusion of carbon dioxide.
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Abbreviations
- APX:
-
Ascorbate peroxidase
- BRs:
-
Brassinosteroids
- CA:
-
Carbonic anhydrase
- CAR:
-
Carotenoids
- CAT:
-
Catalase
- Chl a :
-
Chlorophyll a
- Chl b :
-
Chlorophyll b
- C i :
-
Intercellular CO2 concentration
- CO2 :
-
Carbon dioxide
- E :
-
Transpiration rate
- EBR:
-
24-epibrassinolide
- EDS:
-
Equatorial diameter of the stomata
- EL:
-
Electrolyte leakage
- ETAb:
-
Epidermis thickness from abaxial leaf side
- ETAd:
-
Epidermis thickness from adaxial leaf side
- ETR:
-
Electron transport rate
- ETR/PN :
-
Ratio between the apparent electron transport rate and net photosynthetic rate
- EXC:
-
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
- g s :
-
Stomatal conductance
- H2O2 :
-
Hydrogen peroxide
- LDM:
-
Leaf dry matter
- MDA:
-
Malondialdehyde
- NPQ:
-
Nonphotochemical quenching
- O2− :
-
Superoxide
- PDS:
-
Polar diameter of the stomata
- P N :
-
Net photosynthetic rate
- PN/Ci :
-
Instantaneous carboxylation efficiency
- POX:
-
Peroxidase
- PPT:
-
Palisade parenchyma thickness
- PSII:
-
Photosystem II
- qP :
-
Photochemical quenching
- RCD:
-
Root cortex diameter
- RDM:
-
Root dry matter
- RMD:
-
Root metaxylem diameter
- RDT:
-
Root endodermis thickness
- RET:
-
Root epidermis thickness
- ROS:
-
Reactive oxygen species
- RuBisCO:
-
Ribulose-1,5-bisphosphate carboxylase/oxygenase
- SD:
-
Stomatal density
- SDM:
-
Stem dry matter
- SF:
-
Stomatal functionality
- SI:
-
Stomatal index
- SOD:
-
Superoxide dismutase
- SPT:
-
Spongy parenchyma thickness
- TDM:
-
Total dry matter
- Total Chl:
-
Total Chlorophyll
- VCD:
-
Vascular cylinder diameter
- WUE:
-
Water-use efficiency
- ΦPSII :
-
Effective quantum yield of PSII photochemistry
References
Abdullahi BA, Gu X, Gan Q, Yang Y (2003) Brassinolide amelioration of aluminum toxicity in mungbean seedling growth. J Plant Nutr 26:1725–1734. https://doi.org/10.1081/PLN-120023278
Abreu IA, Cabelli DE (2010) Superoxide dismutases—a review of the metal-associated mechanistic variations. Biochim Biophys Acta, Proteins Proteomics 1804:263–274. https://doi.org/10.1016/j.bbapap.2009.11.005
Ahammed GJ, Choudhary SP, Chen S et al (2013) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213. https://doi.org/10.1093/jxb/ers323
Allen LH Jr, Zhang L, Boote KJ, Hauser BA (2018) Elevated temperature intensity, timing, and duration of exposure affect soybean internode elongation, mainstem node number, and pod number per plant. Crop J 6:148–161. https://doi.org/10.1016/j.cj.2017.10.005
Alyemeni MN, Al-Quwaiz SM (2016) Effect of 28-homobrassinolide on the performance of sensitive and resistant varieties of Vigna radiata. Saudi J Biol Sci 23:698–705. https://doi.org/10.1016/j.sjbs.2016.01.002
Andrejić G, Gajić G, Prica M, Dželetović Ž, Rakić T (2018) Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus × giganteus plants. Photosynthetica 56:1249–1258. https://doi.org/10.1007/s11099-018-0827-3
Antoniadis V, Shaheen SM, Tsadilas CD et al (2018) Zinc sorption by different soils as affected by selective removal of carbonates and hydrous oxides. Appl Geochem 88:49–58. https://doi.org/10.1016/j.apgeochem.2017.04.007
Anwar A, Liu Y, Dong R, Bai L, Yu X, Li Y (2018) The physiological and molecular mechanism of brassinosteroid in response to stress: a review. Biol Res 51:1–15. https://doi.org/10.1186/s40659-018-0195-2
Aragão RM, Silva EN, Vieira CF, Silveira JAG (2012) High supply of NO3 − mitigates salinity effects through an enhancement in the efficiency of photosystem II and CO2 assimilation in Jatropha curcas plants. Acta Physiol Plant 34:2135–2143. https://doi.org/10.1007/s11738-012-1014-y
Arrivault S, Senger T, Krämer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879. https://doi.org/10.1111/j.1365-313X.2006.02746.x
Azhar N, Su N, Shabala L, Shabala S (2017) Exogenously applied 24-epibrassinolide (EBL) ameliorates detrimental effects of salinity by reducing K+ efflux via depolarization-activated K+ channels. Plant Cell Physiol 58:802–810. https://doi.org/10.1093/pcp/pcx026
Azzarello E, Pandolfi C, Giordano C et al (2012) Ultramorphological and physiological modifications induced by high zinc levels in Paulownia tomentosa. Environ Exp Bot 81:11–17. https://doi.org/10.1016/j.envexpbot.2012.02.008
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. https://doi.org/10.1016/j.plantsci.2003.12.007
Baig MA, Ahmad J, Bagheri R, Ali AA, al-Huqail AA, Ibrahim MM, Qureshi MI (2018) Proteomic and ecophysiological responses of soybean (Glycine max L.) root nodules to Pb and hg stress. BMC Plant Biol 18:283–221. https://doi.org/10.1186/s12870-018-1499-7
Bajguz A (2000) Effect of brassinosteroids on nucleic acids and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215. https://doi.org/10.1016/S0981-9428(00)00733-6
Bajguz A (2010) An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ Exp Bot 68:175–179. https://doi.org/10.1016/j.envexpbot.2009.11.003
Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8. https://doi.org/10.1016/j.plaphy.2008.10.002
Balasaraswathi K, Jayaveni S, Sridevi J et al (2017) Cr–induced cellular injury and necrosis in Glycine max L.: biochemical mechanism of oxidative damage in chloroplast. Plant Physiol Biochem 118:653–666. https://doi.org/10.1016/j.plaphy.2017.08.001
Barberon M, Vermeer JEM, De Bellis D et al (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164:447–459. https://doi.org/10.1016/j.cell.2015.12.021
Bazihizina N, Taiti C, Marti L et al (2014) Zn2+−induced changes at the root level account for the increased tolerance of acclimated tobacco plants. J Exp Bot 65:4931–4942. https://doi.org/10.1093/jxb/eru251
Billard V, Maillard A, Garnica M et al (2015) Zn deficiency in Brassica napus induces Mo and Mn accumulation associated with chloroplast proteins variation without Zn remobilization. Plant Physiol Biochem 86:66–71. https://doi.org/10.1016/j.plaphy.2014.11.005
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. https://doi.org/10.1016/0003-2697(76)90527-3
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. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
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. https://doi.org/10.1104/pp.98.4.1222
Casson SA, Hetherington AM (2012) GSK3-like kinases integrate brassinosteroid signaling and stomatal development. Sci Signal 5:1–3. https://doi.org/10.1126/scisignal.2003311
Castro EM, Pereira FJ, Paiva R (2009) Plant histology: structure and function of vegetative organs. Lavras
Cui H (2015) Cortex proliferation in the root is a protective mechanism against abiotic stress. Plant Signal Behav 10:e1011949. https://doi.org/10.1080/15592324.2015.1011949
Dobrikova AG, Vladkova RS, Rashkov GD et al (2014) Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions. Plant Physiol Biochem 80:75–82. https://doi.org/10.1016/j.plaphy.2014.03.022
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620. https://doi.org/10.1016/0003-2697(76)90488-7
Ennajeh M, Vadel AM, Cochard H, Khemira H (2010) Comparative impacts of water stress on the leaf anatomy of a drought-resistant and a drought-sensitive olive cultivar. J Hortic Sci Biotechnol 85:289–294. https://doi.org/10.1080/14620316.2010.11512670
Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351. https://doi.org/10.1007/s00344-003-0002-2
Fan M, Zhu J, Richards C et al (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Funct Plant Biol 30:493–506. https://doi.org/10.1071/FP03046
FAO (2018) Food and agriculture organization of the united nations. Food outlook: Biannual report on global food markets. FAO, Rome
Fei X, Xing-zheng F, Nan-qi W et al (2016) Physiological changes and expression characteristics of ZIP family genes under zinc deficiency in navel orange (Citrus sinensis). J Integr Agric 15:803–811. https://doi.org/10.1016/S2095-3119(15)61276-X
Fiedor L, Kania A, Mysliwa-Kurdziel B et al (2008) Understanding chlorophylls: central magnesium ion and phytyl as structural determinants. Biochim Biophys Acta Bioenerg 1777:1491–1500. https://doi.org/10.1016/j.bbabio.2008.09.005
Flexas J, Ribas-carbó M, Diaz-espejo A et al (2008) Mesophyll conductance to CO 2 : current knowledge and future prospects. Plant Cell Environ 31:602–621. https://doi.org/10.1111/j.1365-3040.2007.01757.x
Flexas J, Barbour MM, Brendel O et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84. https://doi.org/10.1016/j.plantsci.2012.05.009
Fu C, Li M, Zhang Y et al (2015) Morphology, photosynthesis, and internal structure alterations in field apple leaves under hidden and acute zinc deficiency. Sci Hortic (Amsterdam) 193:47–54. https://doi.org/10.1016/j.scienta.2015.06.016
Gallego SM, Pena LB, Barcia RA et al (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46. https://doi.org/10.1016/j.envexpbot.2012.04.006
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314
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. https://doi.org/10.1016/S0176-1617(98)80179-X
Hafeez B, Khanif YM, Saleem M (2013) Role of zinc in plant nutrition- a review. Am J Exp Agric 3:374–391. https://doi.org/10.9734/AJEA/2013/2746
Hajiboland R, Amirazad F (2010) Growth, photosynthesis and antioxidant defense system in Zn-deficient red cabbage plants. Plant Soil Environ 56:209–217
Hameed M, Ashraf M, Naz N (2009) Anatomical adaptations to salinity in cogon grass [Imperata cylindrica (L.) Raeuschel] from the salt range, Pakistan. Plant Soil 322:229–238. https://doi.org/10.1007/s11104-009-9911-6
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (cu, Zn, Mn, Fe, Ni, Mo, B, cl). Curr Opin Plant Biol 12:259–266. https://doi.org/10.1016/j.pbi.2009.05.006
Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451. https://doi.org/10.1016/j.chemosphere.2011.04.047
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450
Hayat S, Yadav S, Wani AS et al (2011) Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the growth, carbonic anhydrase activity and photosynthetic efficiency of Lycopersicon esculentum. Photosynthetica 49:397–404. https://doi.org/10.1007/s11099-011-0051-x
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 19:325–335
He J, Wang Y, Ding H, Ge C (2016) Epibrassinolide confers zinc stress tolerance by regulating antioxidant enzyme responses, osmolytes, and hormonal balance in Solanum melongena seedlings. Brazilian J Bot 39:295–303. https://doi.org/10.1007/s40415-015-0210-6
Hidoto L, Worku W, Mohammed H, Taran B (2017) Effects of zinc application strategy on zinc content and productivity of chickpea grown under zinc deficient soils. J Soil Sci Plant Nutr 17:112–126. https://doi.org/10.4067/S0718-95162017005000009
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, 2nd edn. California Agricultural Experiment Station, Riverside
Jain R, Srivastava S, Solomon S et al (2010) Impact of excess zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pigments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiol Plant 32:979–986. https://doi.org/10.1007/s11738-010-0487-9
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39. https://doi.org/10.1111/j.1469-8137.2010.03514.x
Jia L, Liu Z, Chen W et al (2015) Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. J Plant Growth Regul 34:13–21. https://doi.org/10.1007/s00344-014-9433-1
Jiang YP, Cheng F, Zhou YH et al (2012) Interactive effects of CO2 enrichment and brassinosteroid on CO2 assimilation and photosynthetic electron transport in Cucumis sativus. Environ Exp Bot 75:98–106. https://doi.org/10.1016/j.envexpbot.2011.09.002
Karlidag H, Yildirim E, Turan M (2011) Role of 24-epibrassinolide in mitigating the adverse effects of salt stress on stomatal conductance, membrane permeability, and leaf water content, ionic composition in salt stressed strawberry (Fragaria×ananassa). Sci Hortic (Amsterdam) 130:133–140. https://doi.org/10.1016/j.scienta.2011.06.025
Khodamoradi K, Khoshgoftarmanesh AH, Dalir N et al (2015) How do glycine and histidine in nutrient solution affect zinc uptake and root-to-shoot translocation by wheat and triticale? Crop Pasture Sci 66:1105. https://doi.org/10.1071/CP14227
Kim T, Wetzstein HY (2003) Cytological and ultrastructural evaluations of zinc deficiency in leaves. J Am Soc Hortic Sci 128:171–175. https://doi.org/10.21273/JASHS.128.2.0171
Kim T-W, Michniewicz M, Bergmann DC, Wang Z-Y (2012) Brassinosteroid regulates stomatal development by GSK3- mediated inhibition of a MAPK pathway. Nature 482:419–422. https://doi.org/10.1038/nature10794.Brassinosteroid
Kosesakal T, Unal M (2009) Role of zinc deficiency in photosynthentic pigments and peroxidase activity of tomato seedlings. Istanbul Univ Fac Sci J Biol 68:113–120
Kozhevnikova AD, Seregin IV, Erlikh NT et al (2014) Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 203:508–519. https://doi.org/10.1111/nph.12816
Kumari A, Sheokand S, Swaraj K (2010) Nitric oxide induced alleviation of toxic effects of short term and long term cd stress on growth, oxidative metabolism and cd accumulation in chickpea. Braz J Plant Physiol 22:271–284. https://doi.org/10.1590/S1677-04202010000400007
Kunert KJ, Vorster BJ, Fenta BA et al (2016) Drought stress responses in soybean roots and nodules. Front Plant Sci 7:1–7. https://doi.org/10.3389/fpls.2016.01015
Li M, Ahammed GJ, Li C et al (2016a) Brassinosteroid ameliorates zinc oxide nanoparticles-induced oxidative stress by improving antioxidant potential and redox homeostasis in tomato seedling. Front Plant Sci 7:1–13. https://doi.org/10.3389/fpls.2016.00615
Li X, Guo X, Zhou Y et al (2016b) Overexpression of a brassinosteroid biosynthetic gene dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato. BMC Plant Biol 16:33–12. https://doi.org/10.1186/s12870-016-0715-6
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Current protocols in food analytical chemistry. Wiley, Hoboken, pp 431–438
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. https://doi.org/10.1007/s12298-016-0410-y
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 32:1681–1694. https://doi.org/10.1007/s00468-018-1743-7
Lynch JP (2007) Rhizoeconomics: the roots of shoot growth limitations. Hortscience 42:1107–1109
Ma JF, Mitani N, Nagao S et al (2004) Characterization of the silicon uptake system and molecular mapping of the silicon transporter gene in rice. Plant Physiol 136:3284–3289. https://doi.org/10.1104/pp.104.047365
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. https://doi.org/10.1007/s00344-018-9802-2
Manaf A, Raheel M, Sher A et al (2019) Interactive effect of zinc fertilization and cultivar on yield and nutritional attributes of canola (Brassica napus L.). J Soil Sci Plant Nutr 19:in press. https://doi.org/10.1007/s42729-019-00067-2
Marques MC, Nascimento CWA, da Silva AJ, da Silva G-NA (2017) Tolerance of an energy crop (Jatropha curcas L.) to zinc and lead assessed by chlorophyll fluorescence and enzyme activity. South African J Bot 112:275–282. https://doi.org/10.1016/j.sajb.2017.06.009
Martins JPR, Verdoodt V, Pasqual M, De Proft M (2015) Impacts of photoautotrophic and photomixotrophic conditions on in vitro propagated Billbergia zebrina (Bromeliaceae). Plant Cell Tissue Organ Cult 123:121–132. https://doi.org/10.1007/s11240-015-0820-5
Mateos-Naranjo E, Pérez-Romero JA, Redondo-Gómez S et al (2018) Salinity alleviates zinc toxicity in the saltmarsh zinc-accumulator Juncus acutus. Ecotoxicol Environ Saf 163:478–485. https://doi.org/10.1016/j.ecoenv.2018.07.092
Mattiello EM, Ruiz HA, Neves JCL et al (2015) Zinc deficiency affects physiological and anatomical characteristics in maize leaves. J Plant Physiol 183:138–143. https://doi.org/10.1016/j.jplph.2015.05.014
Meyer CJ, Peterson CA, Steudle E (2011) Permeability of Iris germanica’s multiseriate exodermis to water, NaCl, and ethanol. J Exp Bot 62:1911–1926. https://doi.org/10.1093/jxb/erq380
Müssig C (2005) Brassinosteroid-promoted growth. Plant Biol 7:110–117. https://doi.org/10.1055/s-2005-837493
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nisa Z, Chen C, Yu Y et al (2016) Constitutive overexpression of myo-inositol-1-phosphate synthase gene (GsMIPS2) from Glycine soja confers enhanced salt tolerance at various growth stages in Arabidopsis. J Northeast Agric Univ (English Ed 23:28–44. https://doi.org/10.1016/S1006-8104(16)30045-9
Noulas C, Tziouvalekas M, Karyotis T (2018) Zinc in soils, water and food crops. J Trace Elem Med Biol 49:252–260. https://doi.org/10.1016/j.jtemb.2018.02.009
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373
Ogweno JO, Song XS, Shi K et al (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57. https://doi.org/10.1007/s00344-007-9030-7
Oh K, Yamada K, Asami T, Yoshizawa Y (2012) Synthesis of novel brassinosteroid biosynthesis inhibitors based on the ketoconazole scaffold. Bioorg Med Chem Lett 22:1625–1628. https://doi.org/10.1016/j.bmcl.2011.12.120
Oliveira VP, Lima MDR, Silva BRS et al (2019) Brassinosteroids confer tolerance to salt stress in Eucalyptus urophylla plants enhancing homeostasis, antioxidant metabolism and leaf anatomy. J Plant Growth Regul 19 In press. https://doi.org/10.1007/s00344-018-9870-3
Ouni Y, Mateos-Naranjo E, Abdelly C, Lakhdar A (2016) Interactive effect of salinity and zinc stress on growth and photosynthetic responses of the perennial grass, Polypogon monspeliensis. Ecol Eng 95:171–179. https://doi.org/10.1016/j.ecoleng.2016.06.067
Palmer CM, Guerinot ML (2009) Facing the challenges of cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340. https://doi.org/10.1038/nchembio.166
Pascual MB, Echevarria V, Gonzalo MJ, Hernández-Apaolaza L (2016) Silicon addition to soybean (Glycine max L.) plants alleviate zinc deficiency. Plant Physiol Biochem 108:132–138. https://doi.org/10.1016/j.plaphy.2016.07.008
Pereira YC, Rodrigues WS, Lima EJA et al (2019) Brassinosteroids increase electron transport and photosynthesis in soybean plants under water deficit. Photosynthetica 57:1–11
Postma JA, Lynch JP (2011) Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiol 156:1190–1201. https://doi.org/10.1104/pp.111.175489
Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:1–5. https://doi.org/10.3389/fpls.2016.00629
Ramakrishna B, Rao SSR (2012) 24-Epibrassinolide alleviated zinc-induced oxidative stress in radish (Raphanus sativus L.) seedlings by enhancing antioxidative system. Plant Growth Regul 68:249–259. https://doi.org/10.1007/s10725-012-9713-3
Ramakrishna B, Rao SSR (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252:665–677. https://doi.org/10.1007/s00709-014-0714-0
Reis AR, Lisboa LAM, Reis HPG et al (2018) Depicting the physiological and ultrastructural responses of soybean plants to Al stress conditions. Plant Physiol Biochem 130:377–390. https://doi.org/10.1016/j.plaphy.2018.07.028
Rezapour S, Golmohammad H, Ramezanpour H (2014) Impact of parent rock and topography aspect on the distribution of soil trace metals in natural ecosystems. Int J Environ Sci Technol 11:2075–2086. https://doi.org/10.1007/s13762-014-0663-3
Sadeghzadeh B (2013) A review of zinc nutrition and plant breeding. J Soil Sci Plant Nutr 13:905–927. https://doi.org/10.4067/S0718-95162013005000072
Saengwilai P, Nord EA, Chimungu JG et al (2014) Root cortical aerenchyma enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166:726–735. https://doi.org/10.1104/pp.114.241711
Sagardoy R, Morales F, López-Millán AF et al (2009) Effects of zinc toxicity on sugar beet ( Beta vulgaris L.) plants grown in hydroponics. Plant Biol 11:339–350. https://doi.org/10.1111/j.1438-8677.2008.00153.x
Salama ZA, El-Fouly MM, Lazova G, Popova LP (2006) Carboxylating enzymes and carbonic anhydrase functions were suppressed by zinc deficiency in maize and chickpea plants. Acta Physiol Plant 28:445–451. https://doi.org/10.1007/BF02706627
Samreen T, Humaira, Shah HU et al (2017) Zinc effect on growth rate, chlorophyll, protein and mineral contents of hydroponically grown mungbeans plant (Vigna radiata). Arab J Chem 10:S1802–S1807. https://doi.org/10.1016/j.arabjc.2013.07.005
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. https://doi.org/10.1016/j.plaphy.2017.01.022
Santos LR, Batista BL, Lobato AKS (2018) Brassinosteroids mitigate cadmium toxicity in cowpea plants. Photosynthetica 56:591–605. https://doi.org/10.1007/s11099-017-0700-9
Schneider HM, Wojciechowski T, Postma JA et al (2017) Root cortical senescence decreases root respiration, nutrient content and radial water and nutrient transport in barley. Plant Cell Environ 40:1392–1408. https://doi.org/10.1111/pce.12933
Segatto FB, Bisognin DA, Benedetti M et al (2004) A technique for the anatomical study of potato leaf epidermis. Ciência Rural 34:1597–1601. https://doi.org/10.1590/S0103-84782004000500042
Shahbaz M, Ashraf M, Athar H-U-R (2008) Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? Plant Growth Regul 55:51–64. https://doi.org/10.1007/s10725-008-9262-y
Shu S, Tang Y, Yuan Y et al (2016) The role of 24-epibrassinolide in the regulation of photosynthetic characteristics and nitrogen metabolism of tomato seedlings under a combined low temperature and weak light stress. Plant Physiol Biochem 107:344–353. https://doi.org/10.1016/j.plaphy.2016.06.021
Shu K, Qi Y, Chen F et al (2017) Salt stress represses soybean seed germination by negatively regulating GA biosynthesis while positively mediating ABA biosynthesis. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.01372
Siddiqui H, Ahmed KBM, Hayat S (2018) Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the performance of different components influencing the photosynthetic machinery in Brassica juncea L. Plant Physiol Biochem 129:198–212. https://doi.org/10.1016/j.plaphy.2018.05.027
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. https://doi.org/10.1016/j.biombioe.2012.06.009
Sinclair SA, Krämer U (2012) The zinc homeostasis network of land plants. Biochim Biophys Acta, Mol Cell Res 1823:1553–1567. https://doi.org/10.1016/j.bbamcr.2012.05.016
Singh HP, Batish DR, Kohli RK, Arora K (2007) Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53:65–73. https://doi.org/10.1007/s10725-007-9205-z
Singh P, Kumar R, Sabapathy SN, Bawa AS (2008) Functional and edible uses of soy protein products. Compr Rev Food Sci Food Saf 7:14–28. https://doi.org/10.1111/j.1541-4337.2007.00025.x
Singh P, Shukla AK, Behera SK, Tiwari PK (2019) Zinc application enhances superoxide dismutase and carbonic anhydrase activities in zinc-efficient and zinc-inefficient wheat genotypes. J soil Sci plant Nutr 19:in press. https://doi.org/10.1007/s42729-019-00038-7
Steel RG, Torrie JH, Dickey DA (2006) Principles and procedures of statistics: a biometrical approach, 3rd edn. Academic Internet Publishers, Moorpark
Subba P, Mukhopadhyay M, Mahato SK, Bhutia KD, Mondal TK, Ghosh SK (2014) Zinc stress induces physiological, ultra-structural and biochemical changes in mandarin orange (Citrus reticulata Blanco) seedlings. Physiol Mol Biol Plants 20:461–473. https://doi.org/10.1007/s12298-014-0254-2
Suhr N, Schoenberg R, Chew D et al (2018) Elemental and isotopic behaviour of Zn in Deccan basalt weathering profiles: chemical weathering from bedrock to laterite and links to Zn deficiency in tropical soils. Sci Total Environ 619–620:1451–1463. https://doi.org/10.1016/j.scitotenv.2017.11.112
Swamy KN, Rao SSR (2009) Effect of 24-epibrassinolide on growth, photosynthesis, and essential oil content of Pelargonium graveolens (L.) Herit. Russ J Plant Physiol 56:616–620. https://doi.org/10.1134/S1021443709050057
Tadayon MS, Moafpourian G (2019) Effects of exogenous epi-brassinolid, zinc and boron foliar nutrition on fruit development and ripening of grape (Vitis vinifera L. clv. “Khalili”). Sci Hortic (Amsterdam) 244:94–101. https://doi.org/10.1016/j.scienta.2018.09.036
Talukdar D (2013) Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol Mol Biol Plants 19:69–79. https://doi.org/10.1007/s12298-012-0140-8
Tanaka N, Kato M, Tomioka R et al (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 65:1497–1512. https://doi.org/10.1093/jxb/eru014
Tavallali V, Rahemi M, Maftoun M et al (2009) Zinc influence and salt stress on photosynthesis, water relations, and carbonic anhydrase activity in pistachio. Sci Hortic (Amsterdam) 123:272–279. https://doi.org/10.1016/j.scienta.2009.09.006
Thussagunpanit J, Jutamanee K, Sonjaroon W et al (2015) Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. Photosynthetica 53:312–320. https://doi.org/10.1007/s11099-015-0106-5
Tripathi DK, Singh S, Singh S, Mishra S, Chauhan DK, Dubey NK (2015) Micronutrients and their diverse role in agricultural crops: advances and future prospective. Acta Physiol Plant 37:14–14. https://doi.org/10.1007/s11738-015-1870-3
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. https://doi.org/10.1016/S0168-9452(99)00197-1
Wang X, Zhao X, Jiang C et al (2015) Effects of potassium deficiency on photosynthesis and photoprotection mechanisms in soybean (Glycine max (L.) Merr.). J Integr Agric 14:856–863. https://doi.org/10.1016/S2095-3119(14)60848-0
Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and Symbiosis. Mol Plant 9:86–100. https://doi.org/10.1016/j.molp.2015.12.003
Wijewardana C, Reddy KR, Bellaloui N (2019) Soybean seed physiology, quality, and chemical composition under soil moisture stress. Food Chem 278:92–100. https://doi.org/10.1016/j.foodchem.2018.11.035
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. https://doi.org/10.1016/j.jplph.2005.09.001
Xia X-J, Huang L-F, Zhou Y-H et al (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196. https://doi.org/10.1007/s00425-009-1016-1
Yu JQ, Huang L-F, Hu WH et al (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143. https://doi.org/10.1093/jxb/erh124
Yuan L, Zhu S, Shu S et al (2015) Regulation of 2,4-epibrassinolide on mineral nutrient uptake and ion distribution in Ca(NO3)2 stressed cucumber plants. J Plant Physiol 188:29–36. https://doi.org/10.1016/j.jplph.2015.06.010
Zhang YP, Zhu XH, Ding HD et al (2013) Foliar application of 24-epibrassinolide alleviates high-temperature-induced inhibition of photosynthesis in seedlings of two melon cultivars. Photosynthetica 51:341–349. https://doi.org/10.1007/s11099-013-0031-4
Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924. https://doi.org/10.1007/s00709-014-0732-y
Zhiponova MK, Vanhoutte I, Boudolf V et al (2013) Brassinosteroid production and signaling differentially control cell division and expansion in the leaf. New Phytol 197:490–502. https://doi.org/10.1111/nph.12036
Acknowledgements
This research had financial supports from Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), Programa de Pós-Graduação em Agronomia (PGAGRO/Brazil) and Universidade Federal Rural da Amazônia (UFRA/Brazil) to AKSL. In other hand, LRS was supported with scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/Brazil).
Author Contribution Statement
AKSL was the advisor of this project, planning all phases of this research. LRS conducted the experiment in the greenhouse and performed physiological, biochemical and morphological determinations, while BRSS measured anatomical parameters. TP and BLB performed nutritional determinations and helped in drafting the manuscript and in interpreting the results.
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Data are available upon request to the corresponding author.
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dos Santos, L.R., da Silva, B.R.S., Pedron, T. et al. 24-Epibrassinolide Improves Root Anatomy and Antioxidant Enzymes in Soybean Plants Subjected to Zinc Stress. J Soil Sci Plant Nutr 20, 105–124 (2020). https://doi.org/10.1007/s42729-019-00105-z
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DOI: https://doi.org/10.1007/s42729-019-00105-z