Influence of copper on hormone content and selected morphological, physiological and biochemical parameters of hydroponically grown Zea mays plants Original paper First Online: 10 August 2019 Abstract
The impact of copper on hydroponically grown
Zea mays L. has been characterized at the level of morphological changes and phytohormones. Maize plants were grown in Hoagland nutrient solution for 14 days with the addition of 50 µM or100 µM CuSO 4. Both the height and the fresh weight of plants were reduced. The hormone analysis, performed by mass spectrometry, revealed elevation of abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA) and indole-3-acetic acid (IAA) in directly exposed roots, only content of active cytokinins (CKs) did not change. In leaves, the content of ABA, JA, IAA and CKs was increased, while the content SA did not change. The content of Ca, Mg, K and Zn decreased in leaves and roots with increasing concentration of Cu in nutrient medium. Leaf Cu concentration decreased at 100 µM CuSO 4 in medium compared to the control (by 48%). Endogenous Cu content highly increased in roots exposed to 50 µM CuSO 4 (by 690%), while only moderate elevation was observed at 100 µM CuSO 4. The content of phenolic substances and flavonoids increased in both roots and leaves, while protein content increased in leaves, not changing in roots. In conclusion, the increase in content of ABA, SA, JA, CKs and IAA in response to elevated Cu concentration in the medium indicated their participation in maize responses to Cu stress. Negative correlation revealed between endogenous Cu and JA or CKs content in leaves suggested their role in reduction of Cu uptake. Keywords Maize Phytohormone Heavy metal Copper Notes Acknowledgements
This work was supported by the Specific Research Project of the Faculty of Science, University of Hradec Kralove, No. 2109/2016 and Ministry of Education, Youth and Sports of CR from the European Regional Development Fund-Project "Centre for Experimental Plant Biology": [Grant No. CZ.02.1.01/0.0/0.0/16_019/0000738]. We would like to thank OSEVA UNI, a.s., Choceň for providing maize seeds.
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Al-Hakimi A-BM, Hamada AM (2011) Ascorbic acid, thiamine or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress. Plant Prot Sci 47:92–108
CrossRef Google Scholar
Argueso CT, Ferreira FJ, Kieber JJ (2009) Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ 32:1147–1160.
https://doi.org/10.1111/j.1365-3040.2009.01940.x CrossRef Google Scholar
Bali S, Kaur P, Kohli SK et al (2018) Jasmonic acid induced changes in physio-biochemical attributes and ascorbate-glutathione pathway in
under lead stress at different growth stages. Sci Total Environ 645:1344–1360.
https://doi.org/10.1016/j.scitotenv.2018.07.164 CrossRef Google Scholar
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488.
https://doi.org/10.1007/s11103-008-9435-0 CrossRef Google Scholar
Benimeli CS, Medina A, Navarro CM et al (2009) Bioaccumulation of copper by
: impact on root, shoot and leaf growth. Water Air Soil Pollut 210:365–370.
https://doi.org/10.1007/s11270-009-0259-6 CrossRef Google Scholar
Bhattarai KK, Xie Q-G, Mantelin S et al (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol Plant-Microbe Interact 21:1205–1214.
https://doi.org/10.1094/MPMI-21-9-1205 CrossRef Google Scholar
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 CrossRef Google Scholar
Bücker-Neto L, Paiva ALS, Machado RD et al (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386.
https://doi.org/10.1590/1678-4685-GMB-2016-0087 CrossRef Google Scholar
Bulak P, Walkiewicz A, Brzezińska M (2014) Plant growth regulators-assisted phytoextraction. Biol Plant 58:1–8.
https://doi.org/10.1007/s10535-013-0382-5 CrossRef Google Scholar
Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z et al (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266.
https://doi.org/10.1016/j.envexpbot.2004.02.004 CrossRef Google Scholar
Di Ferdinando M, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. Springer, New York
CrossRef Google Scholar
Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29.
https://doi.org/10.1016/s0021-9673(02)00024-9 CrossRef Google Scholar
Dobrev P, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 251–261
Elahi N, Rehmani MIA, Majeed A, Ahmad M (2018) Salicylic acid improves physiological traits of
L. seedlings under copper contamination. Asian J Agric Biol 6:115–124
Freitas F, Lunardi S, Souza LB et al (2018) Accumulation of copper by the aquatic macrophyte
Raddi (Salviniaceae). Braz J Biol 78:133–139.
https://doi.org/10.1590/1519-6984.166377 CrossRef Google Scholar
Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420.
https://doi.org/10.1016/j.pbi.2006.05.013 CrossRef Google Scholar
Hąc-Wydro K, Sroka A, Jabłońska K (2016) The impact of auxins used in assisted phytoextraction of metals from the contaminated environment on the alterations caused by lead(II) ions in the organization of model lipid membranes. Colloids Surf B Biointerfaces 143:124–130.
https://doi.org/10.1016/j.colsurfb.2016.03.018 CrossRef Google Scholar
Han Y, Chen G, Chen Y, Shen Z (2015) Cadmium toxicity and alleviating effects of exogenous salicylic acid in iris hexagona. Bull Environ Contam Toxicol 95:796–802.
https://doi.org/10.1007/s00128-015-1640-3 CrossRef Google Scholar
Hanaka A, Lechowski L, Mroczek-Zdyrska M, Strubińska J (2018) Oxidative enzymes activity during abiotic and biotic stresses in
leaves and roots exposed to Cu, methyl jasmonate and Trigonotylus caelestialium. Physiol Mol Biol Plants 24:1–5.
https://doi.org/10.1007/s12298-017-0479-y CrossRef Google Scholar
Jung Y, Ha M, Lee J et al (2015) Metabolite profiling of the response of burdock roots to copper stress. J Agric Food Chem 63:1309–1317.
https://doi.org/10.1021/jf503193c CrossRef Google Scholar
Ke W, Xiong Z-T, Chen S, Chen J (2007) Effects of copper and mineral nutrition on growth, copper accumulation and mineral element uptake in two
populations from a copper mine and an uncontaminated field sites. Environ Exp Bot 59:59–67.
https://doi.org/10.1016/j.envexpbot.2005.10.007 CrossRef Google Scholar
Kereszturi P, Andrasi N, Czudar A et al (2009) Effects of exogenous salicylic acid on growth and catalase enzyme in white mustard seedlings under heavy metal and salt stress. Cereal Res Commun 37:597–600
Lachman J, Dudjak J, Miholova D et al (2005) Effect of cadmium on flavonoid content in young barley (
L.) plants. Plant Soil Environ—UZPI Czech Repub 51(11):513–516.
https://doi.org/10.17221/3625-PSE CrossRef Google Scholar
Liphadzi MS, Kirkham MB, Paulsen GM (2006) Auxin-enhanced root growth for phytoremediation of sewage-sludge amended soil. Environ Technol 27:695–704.
https://doi.org/10.1080/09593332708618683 CrossRef Google Scholar
Liu J, Wang J, Lee S, Wen R (2018) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13:e0203612.
https://doi.org/10.1371/journal.pone.0203612 CrossRef Google Scholar
Liu JJ, Wei Z, Li JH (2014) Effects of copper on leaf membrane structure and root activity of maize seedling. Bot Stud 55:47.
https://doi.org/10.1186/s40529-014-0047-5 CrossRef Google Scholar
Maksymiec W (2011) Effects of jasmonate and some other signalling factors on bean and onion growth during the initial phase of cadmium action. Biol Plant 55:112–118.
https://doi.org/10.1007/s10535-011-0015-9 CrossRef Google Scholar
Maksymiec W, Krupa Z (2007) Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant 51:322–326.
https://doi.org/10.1007/s10535-007-0062-4 CrossRef Google Scholar
Maksymiec W, Wianowska D, Dawidowicz AL et al (2005) The level of jasmonic acid in
plants under heavy metal stress. J Plant Physiol 162:1338–1346.
https://doi.org/10.1016/j.jplph.2005.01.013 CrossRef Google Scholar
Moravcova S, Tuma J, Ducaiova ZK et al (2018) Influence of salicylic acid pretreatment on seeds germination and some defence mechanisms of
plants under copper stress. Plant Physiol Biochem 122:19–30.
https://doi.org/10.1016/j.plaphy.2017.11.007 CrossRef Google Scholar
Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (
L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973.
https://doi.org/10.1007/s10646-013-1073-x CrossRef Google Scholar
Müller B, Sheen J (2007) Advances in cytokinin signaling. Science 318:68–69.
https://doi.org/10.1126/science.1145461 CrossRef Google Scholar
Ouzounidou G, Čiamporová M, Moustakas M, Karataglis S (1995) Responses of maize (
L.) plants to copper stress—I. Growth, mineral content and ultrastructure of roots. Environ Exp Bot 35:167–176.
https://doi.org/10.1016/0098-8472(94)00049-B CrossRef Google Scholar
Palma JM, Sandalio LM, Javier Corpas F et al (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40:521–530.
https://doi.org/10.1016/S0981-9428(02)01404-3 CrossRef Google Scholar
Perez Chaca MV, Vigliocco A, Reinoso H et al (2014) Effects of cadmium stress on growth, anatomy and hormone contents in
(L.) Merr. Acta Physiol Plant 36:2815–2826.
https://doi.org/10.1007/s11738-014-1656-z CrossRef Google Scholar
Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J Cell Mol Biol 32:539–548
CrossRef Google Scholar
Pielichowska M, Wierzbicka M (2004) Uptake and localization of cadmium by
, a cadmium hyperaccumulator. Acta Biol Cracoviensia Ser Bot 46:57–63
Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka-Szelewa E, Bralska M (2018) Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga
. Plant Physiol Biochem 132:535–546.
https://doi.org/10.1016/j.plaphy.2018.09.038 CrossRef Google Scholar
Ribeiro DM, Desikan R, Bright J et al (2009) Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ 32:46–57.
https://doi.org/10.1111/j.1365-3040.2008.01906.x CrossRef Google Scholar
Rubio MI, Escrig I, Martínez-Cortina C et al (1994) Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regul 14:151–157.
https://doi.org/10.1007/BF00025217 CrossRef Google Scholar
Schulz E, Tohge T, Zuther E et al (2016) Flavonoids are determinants of freezing tolerance and cold acclimation in
. Sci Rep 6:34027.
https://doi.org/10.1038/srep34027 CrossRef Google Scholar
Semida WM, Rady MM, Abd El-Mageed TA et al (2015) Alleviation of cadmium toxicity in common bean (
L.) plants by the exogenous application of salicylic acid. J Hortic Sci Biotechnol 90:83–91
CrossRef Google Scholar
Sharma SS, Kumar V (2002) Responses of wild type and abscisic acid mutants of
to cadmium. J Plant Physiol 159:1323–1327.
https://doi.org/10.1078/0176-1617-00601 CrossRef Google Scholar
Sheldon AR, Menzies NW (2005) The effect of copper toxicity on the growth and root morphology of Rhodes Grass (
Knuth.) in resin buffered solution culture. Plant Soil 278:341–349.
https://doi.org/10.1007/s11104-005-8815-3 CrossRef Google Scholar
Sinha P, Shukla AK, Sharma YK (2015) Amelioration of heavy-metal toxicity in cauliflower by application of salicylic acid. Commun Soil Sci Plant Anal 46:1309–1319.
https://doi.org/10.1080/00103624.2015.1033543 CrossRef Google Scholar
Srivastava S, Srivastava AK, Suprasanna P, D’Souza SF (2013) Identification and profiling of arsenic stress-induced microRNAs in
. J Exp Bot 64:303–315.
https://doi.org/10.1093/jxb/ers333 CrossRef Google Scholar
Sugawara S, Mashiguchi K, Tanaka K et al (2015) Distinct characteristics of indole-3-acetic acid and phenylacetic acid, two common auxins in plants. Plant Cell Physiol 56:1641–1654.
https://doi.org/10.1093/pcp/pcv088 CrossRef Google Scholar
Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200.
https://doi.org/10.1038/nature07272 CrossRef Google Scholar
Veselov DS, Kudoyarova GR, Kudryakova NV, Kusnetsov VV (2017) Role of cytokinins in stress resistance of plants. Russ J Plant Physiol 64:15–27.
https://doi.org/10.1134/S1021443717010162 CrossRef Google Scholar
Vishwakarma K, Upadhyay N, Kumar N et al (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci.
https://doi.org/10.3389/fpls.2017.00161 Google Scholar
Wellburn A (1994) The spectral determination of chlorophyll-a and chlorophhyll-B, as well. J Plant Physiol 144:307–313
CrossRef Google Scholar
Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525.
https://doi.org/10.1111/j.1365-3040.2009.02052.x CrossRef Google Scholar
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803.
https://doi.org/10.1146/annurev.arplant.57.032905.105444 CrossRef Google Scholar
Yang Z, Chen J, Dou R et al (2015) Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (
L.) and rice (
L.). Int J Environ Res Public Health 12:15100–15109.
https://doi.org/10.3390/ijerph121214963 CrossRef Google Scholar
Zhu XF, Wang ZW, Dong F et al (2013) Exogenous auxin alleviates cadmium toxicity in
by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater 263 Pt 2:398–403.
https://doi.org/10.1016/j.jhazmat.2013.09.018 CrossRef Google Scholar Copyright information
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