Skip to main content
SpringerLink
Log in

Brassinosteroids mitigate cadmium toxicity in cowpea plants

  • Original paper
  • Published:
Photosynthetica

Abstract

Anthropogenic activities and improper uses of phosphate fertilizers have led to an increase in cadmium concentrations in agricultural soils. Brassinosteroids are steroid hormones that are rapidly assimilated and metabolised with beneficial roles in physiological and biochemical processes in plants. Our aim was to ascertain whether exogenous treatment with 24-epibrassinolide (EBR) can mitigate the Cd toxicity, and whether this substance can reduce the Cd accumulation in plant tissues. Furthermore, the dose response to EBR was determined following exposure to Cd in Vigna unguiculata. The experiment was a completely randomised factorial design with two concentrations of Cd (0 and 500 μM) and three concentrations of EBR (0, 50, and 100 nM). Spraying plants exposed to Cd with EBR significantly reduced the concentrations of Cd and increased nutrient contents in all tissues. The EBR treatment caused significant enhancements in leaf, root, and total dry matter. Foliar application of EBR reduced the negative effects of Cd toxicity on chlorophyll fluorescence and gas exchange parameters. Pretreatment with EBR also increased contents of pigments in plants exposed to Cd, compared with the identical treatments without EBR. Cd elevated contents of oxidant compounds, inducing cell damages, while EBR significantly decreased the concentrations of these compounds. We confirmed that EBR mitigated the negative effects related to Cd toxicity, reduced the absorption and transport of Cd, and increased the contents of essential elements. In plants exposed to Cd, the most apparent dose response was found for 100 nM EBR, with beneficial repercussions on growth, gas exchange, primary photosynthetic processes, and photosynthetic pigments, which were intrinsically connected to lower production of oxidant compounds and cell damage.

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

Similar content being viewed by others

Abbreviations

BCF:

bioconcentration factor

BRs:

brassinosteroids

Car:

carotenoids

Cdns :

Cd concentration in nutritive solution

Cdpt :

Cd concentration in plant tissue

Cds :

Cd concentration in the shoots

Cdr :

Cd concentration in roots

Chl:

chlorophyll

C i :

intercellular CO2 concentration

DAE:

day of experiment

E :

transpiration rate

EBR:

24-epibrassinolide

EL:

electrolyte leakage

ETR:

electron transport rate

ETR/P N :

ratio between the apparent electron-transport rate and net photosynthetic rate

EXC:

relative energy excess at the PSII level

Fm :

maximal fluorescence yield of the dark-adapted state

F0 :

minimal fluorescence yield of the dark-adapted state

Fv :

variable fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

FM:

fresh mass

g s :

stomatal conductance to water vapor

LDM:

leaf dry matter

MDA:

malondialdehyde

NPQ:

nonphotochemical quenching

P N :

net photosynthetic rate

P N/C i :

instantaneous carboxylation efficiency

qP :

photochemical quenching

RDM:

root dry matter

ROS:

reactive oxygen species

STM:

stem dry matter

TF:

translocation factor

TDM:

total dry matter

WUE:

water-use efficiency

ΦPSII :

effective quantum yield of PSII photochemistry;.

References

  • Ahammed G.J., Choudhary S.P., Chen S. et al.: Role of brassinosteroids in alleviation of phenanthrene-cadmium cocontamination-induced-photosynthetic inhibition and oxidative stress in tomato. — J. Exp. Bot. 64: 199–213, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ahammed G.J., Gao C.J., Ogweno J.O. et al.: Brassinosteroids induce plant tolerance against phenanthrene by enhancing degradation and detoxification in Solanum lycopersicum L. — Ecotox. Environ. Safe. 80: 28–36, 2012.

    Article  CAS  Google Scholar 

  • Ahmad P., Nabi G., Ashraf M.: Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. — S. Afr. J. Bot. 77: 36–44, 2011.

    Article  CAS  Google Scholar 

  • Ali E., Maodzeka A., Hussain N. et al.: The alleviation of cadmium toxicity in oilseed rape (Brassica napus) by the application of salicylic acid. — Plant Growth Regul. 75: 641–655, 2015.

    Article  CAS  Google Scholar 

  • Allagulova C.R., Maslennikova D.R., Avalbaev A.M. et al.: Influence of 24-epibrassinolide on growth of wheat plants and the content of dehydrins under cadmium stress. — Russ. J. Plant. Physl+ 62: 465–471, 2015.

    Article  CAS  Google Scholar 

  • Alyemeni M.N., Hayat S., Wijaya L., Anaji A.: Foliar application of 28-homobrassinolide mitigates salinity stress by increasing the efficiency of photosynthesis in Brassica juncea. — Acta Bot. Bras. 27: 502–505, 2013.

    Article  Google Scholar 

  • Anuradha S., Rao S.S.R.: The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. — Plant Soil Environ. 53: 465–472, 2007.

    Article  CAS  Google Scholar 

  • Anuradha S., Rao S.S.R.: Effect of 24-epibrassinolide on the photosynthetic activity of radish plants under cadmium stress. — Photosynthetica 47: 317–320, 2009.

    Article  CAS  Google Scholar 

  • Aragão R.M., Silva E.N., Vieira C.F., Silveira J.A.G.: 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, 2012.

    Article  CAS  Google Scholar 

  • Bajguz A.: 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, 2010.

    Article  CAS  Google Scholar 

  • Bajguz A.: Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. — Arch. Environ. Con. Tox. 60: 406–416, 2011.

    Article  CAS  Google Scholar 

  • Bajguz A., Hayat S.: Effects of brassinosteroids on the plant responses to environmental stresses. — Plant Physiol. Bioch. 47: 1–8, 2009.

    Article  CAS  Google Scholar 

  • Bajguz A., Tretyn A.: The chemical characteristic and distribution of brassinosteroids in plants. — Phytochemistry 62: 1027–1046, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Barbosa M.A.M., Lobato A.K.S., Pereira T.S. et al.: Photosynthesis-involvement in modulation of ascorbate and glutathione in Euterpe oleracea plants exposed to drought. — Not. Bot. Horti Agrobo. 42: 119–127, 2014b.

    CAS  Google Scholar 

  • Barbosa M.R., Silva M.M.A., Willadino L. et al.: [Plant generation and enzymatic detoxification of reactive oxygen species.]. — Ciênc. Rural 44: 453–460, 2014a. [In Portuguese]

    Article  CAS  Google Scholar 

  • Basa B., Lattanzio G., Solti A. et al.: Changes induced by cadmium stress and iron deficiency in the composition and organization of thylakoid complexes in sugar beet (Beta vulgaris L.). — Environ. Exp. Bot. 101: 1–11, 2014.

    Article  CAS  Google Scholar 

  • Batista B.L., Nigar M., Mestrot A. et al.: Identification and quantification of phytochelatins in roots of rice to long-term exposure: evidence of individual role on arsenic accumulation and translocation. — J. Exp. Bot. 65: 1467–1479, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Boutraa T., Akhkha A., Al-Shoaibi A.A., Alhejeli A.M.: Effect of water stress on growth and water use efficiency (WUE) of some wheat cultivars (Triticum durum) grown in Saudi Arabia. — J. Taibah Univ. Sci. 3: 39–48, 2010.

    Article  Google Scholar 

  • Cakmak I., Horst W.J.: Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). — Physiol. Plantarum 83: 463–468, 1991.

    Article  CAS  Google Scholar 

  • Chen X., Wang J., Shi Y. et al.: Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. — Bot. Stud. 52: 41–46, 2011.

    CAS  Google Scholar 

  • Ci D., Jiang D., Dai T. et al.: Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing in cadmium tolerance. — Chemosphere 77: 1620–1625, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Clouse S.D., Sasse J.M.: Brassinosteroids: essential regulators of plant growth and development. — Annu. Rev. Plant Phys. 49: 427–451, 1998.

    Article  CAS  Google Scholar 

  • da Silva L., Marchiori P.E.R., Maciel C.P. et al.: [Photosynthesis, water relations and growth of young coffee plants according to phosphorus availability.]. — Pesqui. Agropecu. Bras. 45: 965–972, 2010. [In Portuguese]

    Article  Google Scholar 

  • de Souza Ferraz R.L., de Melo A.S., Suassuna J.F. et al.: [Gas exchange and photosynthetic efficiency in common bean ecotypes grown in a semiarid environment.]. — Pesqui. Agropecu. Trop. 42: 181–188, 2012. [In Portuguese]

    Article  Google Scholar 

  • de Sousa Paula L.S., do Carmo Silva C.B., de Pinho W.C.S. et al.: Silicon (Si) ameliorates the gas exchange and reduces negative impacts on photosynthetic pigments in maize plants under Zinc (Zn) toxicity. — Aust. J. Crop Sci. 9: 901–908, 2015.

    Google Scholar 

  • Dhir B., Sharmila P., Saradhi P.P., Nasim A.S.: Physiological and antioxidant responses of Salvinia natans exposed to chromiumrich wastewater. — Ecotox. Environ. Safe. 72: 1790–1797, 2009.

    Article  CAS  Google Scholar 

  • Djebali W., Zarrouk M., Brouquisse R. et al.: Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. — Plant Biol. 7: 358–368, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Elstner E.F., Heupel A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. — Anal. Biochem. 70: 616–620, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Fang X.W., Turner N.C., Li F.M. et al.: Caragana korshinskii seedlings maintain positive photosynthesis during short-term, severe drought stress. — Photosynthetica 49: 603–609, 2011.

    Article  CAS  Google Scholar 

  • Farooq M., Wahid A., Basra S.M.A., Islam-ud-Din: Improving water relations and gas exchange with brassinosteroids in rice under drought stress. — J. Agron. Crop. Sci. 195: 262–269, 2009.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Filek M., Kościelniak J., Łabanowska M. et al.: Seleniuminduced protection of photosynthesis activity in rape (Brassica napus) seedlings subjected to cadmium stress. Fluorescence and EPR measurements. — Photosynth. Res. 105: 27–37, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Fridman Y., Savaldi-Goldstein S.: Brassinosteroids in growth control: How, when and where. — Plant Sci. 209: 24–31, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Gallego S.M., Pena L.B., Barcia R.A. et al.: Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. — Environ. Exp. Bot. 83: 33–46, 2012.

    Article  CAS  Google Scholar 

  • Gillet S., Decottignies P., Chardonnet S., Maréchal P.L.: Cadmium response and redoxin targets in Chlamydomonas reinhardtii: a proteomic approach. — Photosynth. Res. 89: 201–211, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Gonçalves J.F., Becker A.G., Cargnelutti D. et al.: Cadmium toxicity causes oxidative stress and induces response of the antioxidant system in cucumber seedlings. — Braz. J. Plant Physiol. 19: 223–232, 2007.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gonzalez-Mendoza D., Espadas y Gil F., Santamaría J.M., Zapata-Perez O.: Multiple effects of cadmium on the photosynthetic apparatus of Avicennia germinans L. as probed by OJIP chlorophyll fluorescence measurements. — Z. Naturforsch. C 62: 265–272, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Grove M.D., Spencer G.F., Rohwedder W.K. et al.: Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. — Nature 281: 216–217, 1979.

    Article  CAS  Google Scholar 

  • Guo B., Liang Y., Zhu Y.: Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? — J. Plant Physiol. 166: 20–31, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Guo Q., Meng L., Mao P.C. et al.: Role of exogenous salicylic acid in alleviating cadmium induced toxicity in Kentucky bluegrass. — Biochem. Syst. Ecol. 50: 269–276, 2013.

    Article  CAS  Google Scholar 

  • Hasan S.A., Hayat S., Ahmad A.: Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. — Chemosphere 84: 1446–1451, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Hasan S.A., Hayat S., Ali B., Ahmad A.: 28-homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. — Environ. Pollut. 151: 60–66, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Haubrick L.L., Assmann S.M.: Brassinosteroids and plant function: some clues, more puzzles. — Plant Cell Environ. 29: 446–457, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Hayat S., Ali B., Hasan S.A., Ahmad A.: Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. — Environ. Exp. Bot. 60: 33–41, 2007.

    Article  CAS  Google Scholar 

  • Hayat S., Alyemeni M.N., Hasan S.A.: Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. — Saudi J. Biol. Sci. 19: 325–335, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayat S., Hasan S.A., Hayat Q., Ahmad A.: Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. — Protoplasma 239: 3–14, 2010b.

    Article  CAS  PubMed  Google Scholar 

  • Hayat S., Hasan S.A., Yusuf M. et al.: 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, 2010a.

    Article  CAS  Google Scholar 

  • Hayat S., Khalique G., Wani A.S. et al.: Protection of growth in response to 28-homobrassinolide under the stress of cadmium and salinity in wheat. — Int. J. Biol. Macromol. 64: 130–136, 2014.

    Article  CAS  PubMed  Google Scholar 

  • He Y.J., Xu R.J., Zhao Y.J.: [Enhancement of senescence by epibrassinolide in leaves of mung bean seedling.]. — Acta Physiol. Sin. 22: 58–62, 1996. [In Chinese]

    CAS  Google Scholar 

  • Hermans C., Chen J., Coppens F. et al.: Low magnesium status in plants enhances tolerance to cadmium exposure. — New Phytol. 192: 428–436, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Hernandez L.E., Carpena-Ruiz R., Gárate A.: Alterations in the mineral nutrition of pea seedlings in exposed to cadmium. — J. Plant Nutr. 19: 1581–1586, 1996.

    Article  CAS  Google Scholar 

  • Hoagland D.R., Arnon D.I.: The Water Culture Method for Growing Plants Without Soil, 2nd ed. Pp. 347. California Agricultural Experiment Station, San Francisco 1950.

    Google Scholar 

  • Irfan M., Ahmad A., Hayat S.: Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. — Saudi J. Biol. Sci. 21: 125–131, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Jain M., Pal M., Gupta P., Gadre R.: Effect of cadmium on chlorophyll biosynthesis and enzymes of nitrogen assimilation in greening maize leaf segments: Role of 2-oxoglutarate. — Indian J. Exp. Biol. 45: 385–389, 2007.

    CAS  PubMed  Google Scholar 

  • Janeczko A., Kościelniak J., Pilipowicz M. et al.: Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. — Photosynthetica 43: 293–298, 2005.

    Article  CAS  Google Scholar 

  • Janicka-Russak M., Kabala K., Burzynski M.: Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. — J. Exp. Bot. 63: 4133–4142, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Januškaitienė I.: Impact of low concentration of cadmium on photosynthesis and growth of pea and barley. — Environ. Res. Eng. Manage. 53: 24–29, 2010.

    Google Scholar 

  • Jia L., Liu Z., Chen W. et al.: Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. — J. Plant Growth Regul. 34: 13–21, 2015.

    Article  CAS  Google Scholar 

  • Jiang X.J., Luo Y.M., Liu Q. et al.: Effects of cadmium on nutrient uptake and translocation by Indian Mustard. — Environ. Geochem. Hlth. 26: 319–324, 2004.

    Article  CAS  Google Scholar 

  • Jones-Held S., VanDoren M., Lockwood T.: Brassinolide application to Lepidium sativum seeds and the effects on seedling growth. — J. Plant Growth Regul. 15: 63–67, 1996.

    Article  CAS  Google Scholar 

  • Krantev A., Yordanova R., Janda T. et al.: Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. — J. Plant Physiol. 165: 920–931, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Kroutil M., Hejtmánková A., Lachman J.: Effect of spring wheat (Triticum aestivum L.) treatment with brassinosteroids on the content of cadmium and lead in plant aerial biomass and grain. — Plant Soil Environ. 56: 43–50, 2010.

    Article  CAS  Google Scholar 

  • Kumari A., Sheokand S., Swaraj K.: 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, 2010.

    Article  Google Scholar 

  • Li Q., Lu Y., Shi Y. et al.: Combined effects of cadmium and fluoranthene on germination, growth and photosynthesis of soybean seedlings. — J. Environ. Sci.-China 25: 1936–1946, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Li X., Zhou Q., Sun X., Ren W.: Effects of cadmium on uptake and translocation of nutrient elements in different welsh onion (Allium fistulosum L.) cultivars. — Food Chem. 194: 101–110, 2016.

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler H.K., Buschmann C.: Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. — Curr. Protoc. Food Anal. Chem. 431–438, 2001.

    Google Scholar 

  • Liu S., Yang R., Pan Y. et al.: Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. — Ecotox. Environ. Safe. 119: 35–46, 2015a.

    Article  CAS  Google Scholar 

  • Lopes Júnior C.A., Mazzafera P., Arruda M.A.Z.: A comparative ionomic approach focusing on cadmium effects in sunflowers (Helianthus annuus L.). — Environ. Exp. Bot. 107: 180–186, 2014.

    Article  CAS  Google Scholar 

  • López-Millán A.F., Sagardoy R., Solanas M. et al.: Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. — Environ. Exp. Bot. 65: 376–385, 2009.

    Article  CAS  Google Scholar 

  • Lösch R.: Plant mitochondrial respiration under the influence of heavy metals. — In: Prasad M.N.V. (ed.): Heavy Metal Stress in Plants: From Biomolecules to Ecosystems, 2nd ed. Pp. 182–200. Springer, Berlin. — Heidelberg 2004.

    Google Scholar 

  • Lu L., Tian S., Zhang M. et al.: The role of Ca pathway in Cd uptake and translocation by the hyperaccumulator Sedum alfredii. — J. Hazard. Mater. 183: 22–28, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Ma C.C., Gao Y.B., Guo H.Y., Wang J.L.: Photosynthesis, transpiration and water use efficiency of Caragana microphylla, C. intermedia and C. korshinskii. — Photosynthetica 42: 65–70, 2004.

    Article  CAS  Google Scholar 

  • Mandava N.B., Sasse J.M., Yopp J.H.: Brassinolide, a growthpromoting steroidal lactone. — Physiol. Plantarum 53: 453–461, 1981.

    Article  CAS  Google Scholar 

  • Miralles-Crespo J., Martínez-López J.A., Franco-Leemhuis J.A., Bañón-Arias S.: Determining freezing injury from changes in chlorophyll fluorescence in potted oleander plants. — HortScience 46: 895–900, 2011.

    Google Scholar 

  • Moradi L., Ehsanzadeh P.: Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. — Photosynthetica 53: 506–518, 2015.

    Article  CAS  Google Scholar 

  • Najeeb U., Jilani G., Ali S. et al.: Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. — J. Hazard. Mater. 186: 565–574, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Nwugo C.C., Huerta A.J.: The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmiumstress. — J. Proteome Res. 10: 518–528, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Palliotti A., Tombesi S., Frioni T. et al.: Physiological parameters and protective energy dissipation mechanisms expressed in the leaves of two Vitis vinifera L. genotypes under multiple summer stresses. — J. Plant Physiol. 185: 84–92, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Perfus-Barbeoch L., Leonhardt N., Vavasseur A., Forestier C.: Heavy metal toxicity: Cadmium permeates through calcium channels and disturbs the plant water status. — Plant J. 32: 539–548, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Pinto A.P., Mota A.M., de Varennes A., Pinto F.C.: Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. — Sci. Total Environ. 326: 239–247, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Pinzón-Torres J.A., Schiavinato M.A.: Growth, photosynthetic and water use efficiency in four tropical tree legume species. — Hoehnea 35: 395–404, 2008.

    Article  Google Scholar 

  • Pipattanawong N., Fujishige N., Yamane K., Ogata R.: Effects of brassinosteroid on vegetative and reproductive growth in two day-neutral strawberries. — J. Jpn. Soc. Hortic. Sci. 65: 651–654, 1996.

    Article  CAS  Google Scholar 

  • Przedpelska-Wasowicz E.M., Wierzbicka M.: Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. — Protoplasma 248: 663–671, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Rady M.M.: Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. — Sci. Hortic.-Amsterdam 129: 232–237, 2011.

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramakrishna B., Rao S.S.R.: Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. — Protoplasma 252: 665–677, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Serrano M., Romero-Puertas M.C., Pazmiño D.M. et al.: Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. — Plant Physiol. 150: 229–243, 2009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rojas-Cifuentes G.A., Johnson B.L., Berti M.T., Norvell W.A.: Zinc fertilization effects on seed cadmium accumulation in oilseed and grain crops grown on North Dakota soils. — Chilean J. Agr. Res. 72: 117–124, 2012.

    Article  Google Scholar 

  • Saidi I., Ayouni M., Dhieb A. et al.: Oxidative damages induced by short-term exposure to cadmium in bean plants: Protective role of salicylic acid. — S. Afr. J. Bot. 85: 32–38, 2013.

    Article  CAS  Google Scholar 

  • Sandalio L.M., Dalurzo H.C., Gómez M. et al.: Cadmiuminduced changes in the growth and oxidative metabolism of pea plants. — J. Exp. Bot. 52: 2115–2126, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Sharma I., Pati P.K., Bhardwaj R.: Regulation of growth and antioxidant enzyme activities by 28-homobrassinolide in seedlings of Raphanus sativus L. under cadmium stress. — Indian J. Biochem. Bio. 47: 172–177, 2010.

    CAS  Google Scholar 

  • Silva E.N., Ribeiro R.V., Ferreira-Silva S.L. et al.: Comparative effects of salinity and water stress on photosynthesis, water relations and growth of Jatropha curcas plants. — J. Arid Environ. 74: 1130–1137, 2010.

    Article  Google Scholar 

  • Silva E.N., Ribeiro R.V., Ferreira-Silva S.L. et al.: Coordinate changes in photosynthesis, sugar accumulation and antioxidative enzymes improve the performance of Jatropha curcas plants under drought stress. — Biomass Bioenerg. 45: 270–279, 2012.

    Article  CAS  Google Scholar 

  • Silva F.A.S., Azevedo C.A.V.: [Assistat computational program version for the Windows operating system.]. — Rev. Bras. Prod. Agroind. 4: 71–78, 2002. [In Portuguese].

    Google Scholar 

  • Silveira F.S., Azzolini M., Divan Jr. A.M.: Scanning cadmium photosynthetic responses of Elephantopus mollis for potential phytoremediation practices. — Water Air Soil Pollut. 226: 359, 2015.

    Article  CAS  Google Scholar 

  • Singh S., Prasad S.M.: Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: Mechanism of toxicity amelioration by kinetin. — Sci. Hortic.-Amsterdam 176: 1–10, 2014.

    Article  CAS  Google Scholar 

  • Sobrino-Plata J., Meyssen D., Cuypers A. et al.: Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. — Plant Soil 377: 369–381, 2014.

    Article  CAS  Google Scholar 

  • Srivastava R.K., Pandey P., Rajpoot R. et al.: Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. — Protoplasma 251: 1047–1065, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Steel R.G.D., Torrie J.H., Dickey D.A.: Principles and Procedures of Statistics: a Biometrical Approach, 3rd ed. Pp. 666. Academic Internet Publishers, Moorpark 2006

    Google Scholar 

  • Tang L., Ying R.R., Jiang D. et al.: Impaired leaf CO2 diffusion mediates Cd-induced inhibition of photosynthesis in the Zn/Cd hyperaccumulator Picris divaricate. — Plant Physiol. Bioch. 73: 70–76, 2013.

    Article  CAS  Google Scholar 

  • Vardhini B.V., Anjum N.A.: Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. — Front. Environ. Sci. 2: 67, 2015.

    Article  Google Scholar 

  • Vardhini B.V., Anuradha S., Rao S.S.R.: Brassinosteroids-a great potential to improve crop productivity. — Indian J. Plant Physiol. 11: 1–12, 2006.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Villiers F., Jourdain A., Bastien O. et al.: Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. — J. Exp. Bot. 63: 1185–1200, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Wael M.S., Mostafa M.R., Taia A.A.E.M. et al.: Alleviation of cadmium toxicity in common bean (Phaseolus vulgaris L.) plants by the exogenous application of salicylic acid. — J. Hortic. Sci. Biotech. 90: 83–91, 2015.

    Article  Google Scholar 

  • Wagner G.J.: Accumulation of cadmium in crop plants and its consequences to human health. — Adv. Agron. 51: 173–212, 1993.

    Article  CAS  Google Scholar 

  • Wahid A., Ghani A., Ali I., Ashraf M.Y.: Effects of cadmium on carbon and nitrogen assimilation in shoots of mungbean [Vigna radiata (L.) Wilczek] seedlings. — J. Agron. Crop. Sci. 193: 357–365, 2007.

    Article  CAS  Google Scholar 

  • Wahid A., Ghani A., Javed F.: Effect of cadmium on photosynthesis, nutrition and growth of mungbean. — Agron. Sustain. Dev. 28: 273–280, 2008.

    Article  CAS  Google Scholar 

  • Wan G., Najeeb U., Jilani G. et al.: Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. — Environ. Sci. Pollut. Res. 18: 1478–1486, 2011.

    Article  CAS  Google Scholar 

  • Wang H., Zhao S.C., Liu R.L. et al.: Changes of photosynthetic activities of maize (Zea mays L.) seedlings in response to cadmium stress. — Photosynthetica 47: 277–283, 2009.

    Article  CAS  Google Scholar 

  • Wang, M., Zou, J., Duan, X. et al.: Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). — Bioresource Technol. 98: 82–88, 2007.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Xie L., Yang C., Wang X.: Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. — J. Exp. Bot. 62: 4495–4506, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D., Chen Z., Sun K. et al.: Effect of cadmium on the physiological parameters and the subcellular cadmium localization in the potato (Solanum tuberosum L.). — Ecotoxicol. Environ. Safe. 97: 147–153, 2013.

    Article  CAS  Google Scholar 

  • Yoon J., Cao X., Zhou Q., Ma L.Q.: Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. — Sci. Total Environ. 368: 456–464, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Yuan G.F., Jia C.G., Li Z. et al.: Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. — Sci. Hortic.-Amsterdam 126: 103–108, 2010.

    Article  CAS  Google Scholar 

  • Zhang S., Zhang H., Qin R. et al.: Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. — Ecotoxicology 18: 814–823, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Zhang X., Gao B., Xia H.: Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. — Ecotox. Environ. Safe. 106: 102–108, 2014.

    Article  CAS  Google Scholar 

  • Zhang Y., Xu S., Yang S., Chen Y.: 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, 2015.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Núcleo de Pesquisa Vegetal Básica e Aplicada, Universidade Federal Rural da Amazônia, Paragominas, Pará, Brazil

    L. R. Santos & A. K. S. Lobato

  2. Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, Santo André, São Paulo, Brazil

    B. L. Batista

Authors
  1. L. R. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. L. Batista
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. K. S. Lobato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. K. S. Lobato.

Additional information

Acknowledgements: This research obtained financial supports from Fundação Amazônia de Amparo a Estudos e Pesquisa (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), and Universidade Federal Rural da Amazônia (UFRA/Brazil) to A.K.S. Lobato, while L.R. Santos was supported by graduate scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, L.R., Batista, B.L. & Lobato, A.K.S. Brassinosteroids mitigate cadmium toxicity in cowpea plants. Photosynthetica 56, 591–605 (2018). https://doi.org/10.1007/s11099-017-0700-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-017-0700-9

Additional key words

Search

Navigation