Photosynthetica 2018, 56(2):591-605 | DOI: 10.1007/s11099-017-0700-9
Brassinosteroids mitigate cadmium toxicity in cowpea plants
- 1 Núcleo de Pesquisa Vegetal Básica e Aplicada, Universidade Federal Rural da Amazônia, Paragominas, Pará, Brazil
- 2 Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, Santo André, São Paulo, Brazil
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.
Keywords: cadmium; chlorophyll; net photosynthetic rate; quantum yield of photosystem II; Vigna unguiculata
Received: June 22, 2016; Accepted: December 16, 2016; Published: June 1, 2018Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- Bajguz A., Hayat S.: Effects of brassinosteroids on the plant responses to environmental stresses. - Plant Physiol. Bioch. 47: 1-8, 2009.
Go to original source...
- Bajguz A., Tretyn A.: The chemical characteristic and distribution of brassinosteroids in plants. - Phytochemistry 62: 1027-1046, 2003.
Go to original source...
- 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.
Go to original source...
- 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]
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- Clouse S.D., Sasse J.M.: Brassinosteroids: essential regulators of plant growth and development. - Annu. Rev. Plant Phys. 49: 427-451, 1998.
Go to original source...
- 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]
- 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]
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- Elstner E.F., Heupel A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- Fridman Y., Savaldi-Goldstein S.: Brassinosteroids in growth control: How, when and where. - Plant Sci. 209: 24-31, 2013.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- Haubrick L.L., Assmann S.M.: Brassinosteroids and plant function: some clues, more puzzles. - Plant Cell Environ. 29: 446-457, 2006.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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]
- Hermans C., Chen J., Coppens F. et al.: Low magnesium status in plants enhances tolerance to cadmium exposure. - New Phytol. 192: 428-436, 2011.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- Januškaitienė I.: Impact of low concentration of cadmium on photosynthesis and growth of pea and barley. - Environ. Res. Eng. Manage. 53: 24-29, 2010.
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- Lichtenthaler H.K., Buschmann C.: Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. - Curr. Protoc. Food Anal. Chem. 431-438, 2001.
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- Mandava N.B., Sasse J.M., Yopp J.H.: Brassinolide, a growthpromoting steroidal lactone. - Physiol. Plantarum 53: 453-461, 1981.
Go to original source...
- 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.
Go to original source...
- Moradi L., Ehsanzadeh P.: Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. - Photosynthetica 53: 506-518, 2015.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- Pinzón-Torres J.A., Schiavinato M.A.: Growth, photosynthetic and water use efficiency in four tropical tree legume species. - Hoehnea 35: 395-404, 2008.
- 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.
Go to original source...
- Przedpelska-Wasowicz E.M., Wierzbicka M.: Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. - Protoplasma 248: 663-671, 2011.
Go to original source...
- 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.
Go to original source...
- Rajewska I., Talarek M., Bajguz A.: Brassinosteroids and response of plants to heavy metals action. - Front. Plant Sci. 7: 629, 2016.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- 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].
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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
- 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.
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- Wagner G.J.: Accumulation of cadmium in crop plants and its consequences to human health. - Adv. Agron. 51: 173-212, 1993.
Go to original source...
- 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.
Go to original source...
- Wahid A., Ghani A., Javed F.: Effect of cadmium on photosynthesis, nutrition and growth of mungbean. - Agron. Sustain. Dev. 28: 273-280, 2008.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
- 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.
Go to original source...
- 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.
Go to original source...
- 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.
Go to original source...