Visn. Hark. nac. agrar. univ., Ser. Biol., 2019, Issue 3 (48), p. 6-27


I.V. Kosakivska, М. М. Shcherbatiuk, V. A. Vasyuk, L. V. Voytenko

Kholodny Institute of Botany
of National Academy of Sciences of Ukraine
(Kyiv, Ukraine)

The review analyzes and summarizes the latest literature on the effect of heavy metals (HM) on plant hormonal systems. HM are natural constituent elements of the Earth's crust. Environmentally harmful human activities have caused significant levels of HM pollution in soil and aquatic resources. Elevated concentrations of HM, both essential and non-essential, can adversely affect growth, biomass accumulation, uptake of other mineral substances, photosynthesis, respiration, and water transport. Plant hormones auxins, gibberellins, cytokinins, abscisic and salicylic acids, ethylene, jasmonates and brassinosteroids regulate growth and development of plants during an entire life cycle, and play a key role in adaptation to abiotic and biotic stressors. Plant hormones act as signaling molecules and stimulate responses to different adverse environmental conditions. Excess concentrations of HM can profoundly affect biosynthesis, transport, localization and conjugation of plant hormones, as well as hormonal signaling pathways and crosstalk. Plant tolerance to HM is formed as the result of direct or indirect action of plant hormones. This review discusses the involvement of individual classes of plant hormones in the adaptation of plants to heavy metals, the role of plant hormones in mitigating damaging effects of reactive oxygen species (ROS) exacerbated by high levels by pollution, the interaction between various hormones, and their effect on plant transcriptomes and proteome. Examples of successful exogenous treatment with hormones to stimulate plant resistance to the negative impact of high concentrations of HM are presented. In summary, a study of the hormonal system of plants improves our understanding of mechanisms of absorption, transport and detoxification of HM.

Key words: heavy metals, auxins, gibberellins, cytokinins, abscisic acid, salicylic acid, ethylene, jasmonates, brassinosteroids, reactive oxygen species, resistance to stress



1. Bilanich M.M. 2008. Modern stage of research of Action of heavy metals as toxic elements for plant. Bull. Precarpathian Nat. Ser. Biology. 7 : 161-175.
2. Belyavskaya N.A., Fediuk O.M., Zolotareva E.K. 2018. Plants and heavy metals: perception and signaling. Bull. Kharkiv Nat. Agrarian Univ. Ser. (Visn. Hark. nac. agrar. univ., Ser. Biol.). 3 (45) : 10-30.
3. Vedenicheva N.P., Kosakivska I.V. 2017. Cytokinins as Regulators of Plant Ontogenesis under Different Growth Conditions. Kyiv : 200 p.
4. Veselov D.S., Kudoyarova G.R., Kudryakova N.V., Kusnetsov V.V. 2017. Role of cytokinins in stress resistance of plants. Russ. J. Plant Physiol. 64 (1) : 15-27.
5. Zhovinsky E.Ya., Kuraeva I.V. 2002. Geochemistry of heavy metals in soils of Ukraine. Kiev : 213 p.
6. Karpets Yu.V., Kolupaev Yu.E., Kosakivska I.V. 2016. Nitric oxide and hydrogen peroxide as signal mediators at induction of heat resistance of wheat plantlets by exogenous jasmonic and salicylic acids. Fiziol. rast. genet. 48 (2) : 158-166.
7. Svitovyi V.M., Gerkiyal O.M., Zhilyak I.D. 2014. Zinc and copper in depleted black soil and winter wheat grown on it. Bull. Dnipropetrovsk State Agrarian and Economic University. 34 : 169-171.
8. Titov A.F., Talanova V.V., Kaznina N.M. 2011. The Physiological Basis of Plant Resistance to Heavy Metals. Petrozavodsk : 71 p.
9. Ackova D.G. 2018. Heavy metals and their general toxicity on plants. Plant Sci. Today. 5 : 14-18.
10. Agami R.A., Mohamed G.F. 2013. Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol. Environment. Saf. 94 : 164-171.
11. Al-Hakimi A.M.A. 2007. Modification of cadmium toxicity in pea seedlings by kinetin. Plant Soil Environ. 53 : 129-135.
12. Anuradha S., Rao S.S.R. 2007. Effect of 24-epibrassinolide on the growth and antioxidant enzyme activities in radish seedlings under lead toxicity. Indian J. Plant Physiol. 12 : 396-400.
13. Arora P., Bhardwaj R. 2010. 24-epibrassinolide induced antioxidative defense system of Brassica juncea L. under Zn metal stress. Physiol. Mol. Biol. Plants. 16 : 285-293.
14. Atici Ö., Agar G., Battal P. 2005. Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biol. Plant. 49 : 215-222.
15. Babenko L.M., Kosakivska I.V., Skaterna T.D. 2015. Jasmonic acid: role in biotechnology and the regulation of plants biochemical processes. Biotechnol. Acta. 8 : 36-51.
16. Bajguz A. 2002. Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J. Plant Physiol. 159 : 321-324.
17. Belkadhi A., Djebali W., Hediji H., Chaibi W. 2016. Cellular and signalling mechanisms supporting Cd-tolerance in salicylic acid treated seedlings. Plant Sci. Today. 3 : 41-47.
18. Besson-Bard A., Gravot A., Richaud P., Auroy P., Taconnat L., Renou J., Pugin A., Wendehenne D. 2009. Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol. 149 : 1302-1315.
19. Burnett E.C., Desikan R., Moser R.C., Neill S.J. 2000. ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA. J. Exp. Bot. 51 : 197-205.
20. Bücker-Neto L., Paiva A.L.S., Machado R.D., Arenhar R.A., Margis-Pinheiro M. 2017. Interactions between plant hormones and heavy metals responses. Gen. Mol. Biol. 40 : 373-386.
21. Camacho-Cristóbal J.J., Martín-Rejano E.M., Herrera-Rodríguez M.B., Navarro-Gochicoa M.T., Rexach J., González-Fontes A. 2015. Boron deficiency inhibits root cell elongation via an ethylene/auxin/ROS-dependent pathway in Arabidopsis seedlings. J. Exp. Bot. 66 : 3831-3840.
22. Cao S., Xu Q., Cao Y., Qian K., An K., Zhu Y., Binzeng H., Zhao H., Kuai B. 2005. Loss-of-function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Physiol. Plant. 123 : 57-66.
23. Cao F., Chen F., Sun H., Zhang G., Chen Z.-H., Wu F. 2014. Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics. 15 : 611-625.
24. Chan Z. 2012. Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. Genomics. 100 : 110-115.
25. Chini A., Gimenez-Ibanez S., Goossens A., Solano R. 2016. Redundancy and specificity in jasmonate signaling. Сurr. Opin. Plant Biol. 33 : 147-156.
26. Choudhary S.P., Kanwar M., Bhardwaj R., Gupta B.D., Gupta R.K. 2011. Epibrassinolide ameliorates Cr (VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere. 84 : 592-600.
27. Colebrook E.H., Thomas S.G., Phillips A.L., Hedden P. 2014. The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217 : 67-75.
28. DalCorso G., Farinati S., Furini A. 2010. Regulatory networks of cadmium stress in plants. Plant Signal. Behav. 5 : 663-667.
29. Danquah A., de Zelicourt A., Colcombet J., Hirt H. 2014. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 32 : 40-52.
30. Dar T.A., Moin U., Khan M.M.A., Hakeem K.R., Jaleel 2015. Jasmonates counter plant stress: A review. Environ. Exp. Bot. 115 : 49-57.
31. Davies P.J. 2010. Plant hormones: biosynthesis, signal transduction, action., revised 3rd edn. Dordrecht, Springer : 743 p.
32. El-Monem A., Sharaf A.E.-M.M., Farghal I.I., Sofy M.R. 2009. Role of gibberellic acid in abolishing the detrimental effects of Cd and Pb on broad bean and lupin plants. Res. J. Agric. Biol. Sci. 5 : 6-13.
33. Emamverdian A., Ding Y., Mokhberdoran F., Xie Y. 2015. Heavy Metal Stress and Some Mechanisms of Plant Defense Response. Sci. World J. 2015 : 1-18.
34. Fariduddin Q., Yusuf M., Hayat S., Ahmad A. 2009. Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ. Exp. Bot. 66 : 418-424.
35. Farooq H., Asghar H.N., Khan M.Y., Saleem Mand Zahir Z.A. 2015. Auxin-mediated growth of rice in cadmium-contaminated soil. Turkish J. For. Agric. 39 : 272-276.
36. Fediuc E., Lips S.H., Erdei L. 2005. O-acetylserine (thiol) lyase activity in Phragmites and Typha plants under cadmium and NaCl stress conditions and the involvement of ABA in the stress response. J. Plant Physiol. 162 : 865-872.
37. Finkelstein R. 2013. Abscisic acid synthesis and response. In: Arabidopsis Book. 11 : e0166.
38. Gantait S., Sinniah U.R., Ali MN, Sahu N.C. 2015. Gibberellins - a multifaceted hormone in plant growth regulatory network. Curr. Protein Pept. Sci. 16 : 406-412.
39. Galvez-Valdivieso G., Fryer M.J., Lawson T., Slattery K., Truman W., Asami T., Davies W.J., Jones A.M., Baker N.R., Mullineaux P.M. 2009. The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell. 21 : 2143-2162.
40. Gangwar S., Singh V.P., Prasad M.S., Maurya J.N. 2010. Modulation of manganese toxicity in Pisum sativum L. seedlings by kinetin. Sci Horticult. 126 : 467-474.
41. Gangwar S., Singh V.P., Srivastava P.K., Maurya J.N. 2011. Modification of chromium (VI) phytotoxicity by exogenous gibberellic acid application in Pisum sativum (L.) seedlings. Acta Physiol. Plant. 33 : 1385-1397.
42. Gemrotová M., Kulkarni M.G., Stirk W.A., Strnad M., Van Staden M., Spichal J.L. 2013. Seedlings of medicinal plants treated with either a cytokinin antagonist (PI-55) or an inhibitor of cytokinin degradation (INCYDE) are protected against the negative effects of cadmium. Plant Growth Regul. 71 : 137-145.
43. Ghavri S.V., Singh R.P. 2012. Growth, biomass production and remediation of copper contamination by Jatropha curcas plant in industrial wasteland soil. J. Environ. Biol. 33 : 207-214.
44. Gupta R., Chakrabarty S. 2013. Gibberellic acid in plant. Plant Signal Behav. 8 : e25504.
45. Gupta D.K., Inouhe M., Rodriguez-Serrano M., Romero-Puertas M.C., Sandalio L.M. 2013. Oxidative stress and arsenic toxicity: Role of NADPH oxidase. Chemosphere. 90 : 1987-1996.
46. Hac-Wydro K., Sroka A., Jablo 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 Surfaces B Biointerfaces. 143 : 124-130.
47. Hanaka A., Wojcik M., Dreslar S., Mroczek-Zdyrska M., Maksymiec W. 2016. Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with copper? Ecotoxol. Environ. Saf. 124 : 480-488.
48. Hasan S.A., Hayat S., Ahmad A. 2011. Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere. 84 : 1446-1451.
49. Hashem H.A. 2014. Cadmium toxicity induces lipid peroxidation and alters cytokinin content and antioxidant enzyme activities in soybean. Botany. 92 : 1-7.
50. Hayat S., Ali B., Hasan S.A., Ahmad A. 2007. Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ. Exp. Bot. 60 : 33-41.
51. Hayat S. 2012. Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J. Biol. Sci. 19 : 325-335.
52. Hsu Y.T., Kao C.H. 2003. Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell Environ. 26 : 867-874.
53. Iglesias M.J., Terrile M.C., Bartoli C.G., D'Ippolito S., Casalongue C.A. 2010. Auxin signalling participates in the adaptive response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol. Biol. 74 : 215-222.
54. Ivanov Y.V., Kartashov A.V., Ivanova A.I., SavochkinV., Kuznetsov V.V. 2016. Effects of zinc on Scots pine (Pinus sylvestris L .) seedlings grown in hydroculture. Plant Physiol. Biochem. 102 : 1-9.
55. Jiao Y., Sun L., Song Y., Wang L., Liu L., Zhang L., Liu B., Li N., Miao C., Hao F. 2013. AtrbohD and AtrbohF positively regulates primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. J. Exp. Bot. 64 : 4183-4192.
56. Kanwar M.K., Bhardwaj R., Chowdhary S.P., Arora P., Sharma P., Kumar S. 2013. Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defence of Brassica plants and in vitro cytotoxicity. Acta Physiol. Plant. 35 : 1351-1362.
57. Kapoor D., Rattan A., Gautam V., Kapoor N., Bhardwaj R., Kapoor D., Rattan A., Gautam V., Kapoor N. 2014. 24-Epibrassinolide mediated changes in photosynthetic pigments and antioxidative defence system of radish seedlings under cadmium and mercury stress. Physiol. Biochem. 10 : 110-121.
58. Keunen E., Schellingen K., Vangronsveld J., Cuypers A. 2016. Ethylene and metal stress: Small molecules, big molecules. Front. Plant Sci. 7 : 23.
59. Khan N.A., Nazar R., Iqbal N., Anjum N.A. 2012. Phytohormones and abiotic stress tolerance in plants. Berlin. Springer Verlag. : 308 p.
60. Khan A.L., Lee I.J. 2013. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol. 13 : 86.
61. Khan M.I.R., Khan N.A. 2014. Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma. 251 : 1007-1019
62. Khan A.L., Waqas M., Hussain J., Al-Harrasi A., Hamayun M., Lee I.J. 2015a. Phytohormones enabled endophytic fungal symbiosis improves aluminum phytoextraction in tolerant Solanum lycopersicum: An examples of Penicillium janthinellum LK5 and comparison with exogenous GA3. J. Hazard. Mater. 295 : 70-78.
63. Khan M.I.R., Nazir F., Asgher M., Per T.S., Khan N.A. 2015b. Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J. Plant Physiol. 173 : 9-18.
64. Kim Y-H., Khan A.L., Kim D.H., Lee S.Y., Kim K-M., Waqas M., Jung H-Y., Shin J.H., Kim J.G., Lee I.J. 2014. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol. 14 : 13.
65. Knetsch M.L.W., Wang M., Snaar-Jagalska E., Heimovaara-Dijkstrab S. 1996. Abscisic acid induces Mitogen-Activated Protein Kinase activation in barley aleurone protoplasts. Plant Cell. 8 : 1061-1067.
66. Kong J., Dong Y., Xu L., Liu S., Bai X. 2014. Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot. Studies. 55 : 9.
67. Khripach V., Zhabinskii V., Groot A.D. 2000. Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for XXI century. Ann. Bot. 86 : 441-447.
68. Lequeux H., Hermans C., Lutts S., Verbruggen N. 2010. Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol. Biochem. 48 : 673-682.
69. Lewis D.R., Negi S., Sukumar P., Munday G.K. 2011. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development. 13 : 3485-
70. Leymarie J., Vitkauskaite G., Hoang H.H., Gendreau E., Chazoule V., Meimoun P., Corbineau F., El-Maarouf-Bouteau H., Bailly C. 2012. Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol. 53 : 96-106.
71. Liphadzi M.S., Kirkham M.B., Paulsen G.M. 2006. Auxin enhanced root growth for phytoremediation of sewage sludge amended soil. Environ. Technol. 27 : 695-704.
72. Ljung K. 2013. Auxin metabolism and homeostasis during plant development. Development. 140 : 943-950.
73. Maksymiec W., Wójcik M., Krupa Z. 2007. Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere. 66 : 421-
74. Maksymiec W. 2007. Signaling responses in plants to heavy metal stress. Acta Physiol. Plant. 29 : 177-
75. Masood A., Iqbal N., Khan N.A. 2012. Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by Sulphur in mustard. Plant Cell Environ. 35 : 524-533.
76. Masood A., Khan M.I.R., Fatma M., Asgher M., Per T.S., Khan N.A. 2016. Involvement of ethylene in gibberellic acid-induced sulfur assimilation, photosynthetic responses, and alleviation of cadmium stress in mustard. Plant Physiol. Biochem. 104 : 1-10.
77. Mathur S., Kalaji H.M., Jajoo A. 2016. Investigation of deleterious effects of chromium phytotoxicity and photosynthesis in wheat plant. Photosynthetica. 54 : 1-9.
78. Maksymiec W. 2011. Effects of jasmonate and some other signaling factors on bean and onion growth during the initial phase of cadmium action. Biol. Plant. 55 : 112-118.
79. Meng H., Hua S., Shamsi I.H., Jilani G., Li Y., Jiang L. 2009. Cadmium- induced stress on the seed germination and seedling growth of Brassica napus and its alleviation through exogenous plant growth regulators. Plant Growth Regul. 58 : 47-59.
80. Metwally A., Finkemeier I., Georgi M., Dietz K.J. 2003. Salicylic acid alleviates the cadmium toxicity in barley (Hordeum vulgare) seedlings. Plant Physiol. 132 : 272-281.
81. Mohan T.C., Castrillo G., Navarro C., Zarco-Fernandez S., Ramireddy E., Mateo C., Zanarreno A.M., Paz-Ares J., Munoz R., Garcia-Mina J.M., Hernandez L.E., Schmulling T., Leyva A. 2016. Cytokinin determines thiol-mediated arsenic tolerance and accumulation. Plant Physiol. 171 : 1418-1426.
82. Monni S., Uhlig C., Hansen E., Magel E. 2001. Ecophysiological responses of Empetrum nigrum to heavy metal pollution. Environ. Pollut. 112 : 121-129.
83. Moya J.L., Ros R.,d Picazo I. 1995. Heavy metal-hormone interactions in rice plants: Effects on growth, net photosynthesis, and carbohydrate distribution. J. Plant Growth Regul. 14 : 61-67.
84. Mukhopadhyay M., Mondal T.K. 2015. Effect of zinc and boron on growth and water relations of Camellia sinensis (L.) O. Kuntze cv. T-78. Natl. Acad. Sci. Lett. 38 : 283-286.
85. Munzuro Ö., Fikriye K.Z., Yahyagil Z. 2008. The abscisic acid levels of wheat (Triticum aestivum L. cv. Çakmak 79) seeds that were germinated under heavy metal (Hg++, Cd++, Cu++) stress. G.U. Journal of Science. 21 : 1-7.
86. Nambara E., Okamoto M., Tatematsu K., Yano R., Seo M., Kamiya Y. 2010. Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 20 : 55-67.
87. Nishiyama R., Watanabe Y., Fujita Y., Le D.T., Kojima M., Werner T., Vankova R., Yamaguchi-Shinozaki K., Shinozaki K., Kakimoto T., Sakakibara H., Schmülling T., Tran L.S. 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell. 23 : 2169-2183.
88. Nomura T., Itouga M., Kojima M., Kato Y., Sakakibara H. 2015. Copper mediates auxin signalling to control cell differentiation in the copper moss Scopelophila cataractae. J. Exp. Bot. 66 : 1205-1213.
89. Olds C.L., Glennon E.K.K., Luckhart S. 2018. Abscisic acid: new perspectives on an ancient universal stress signaling molecule. Microbes and Infection. 34 : 1-40.
90. Opdenakker K., Remans T., Keunen E., Vangronsveld J., Cuypers A. 2012. Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAPKinase transcript levels. Environ. Exp. Bot. 83 : 53-61
91. Ostrowski M., Ciarkowska A., Jakubowska A. 2016. The auxin conjugate indole-3-acetyl-aspartate affects responses to cadmium and salt stress in Pisum sativum L. J. Plant Physiol. 191 : 63-72.
92. Pandey C., Gupta M. 2015. Selenium and auxin mitigates arsenic stress in rice (Oryza sativa L.) by combining the role of stress indicators, modulators and genotoxicity assay. J. Hazard Mater. 287 : 384-391.
93. Pandolfini T., Gabbrielli R., Ciscato M. 1996. Nickel toxicity in two durum wheat cultivars differing in drought sensitivity. J. Plant Nutr. 19 : 1611-1627.
94. Pantin F., Monnet F., Jannaud D., Costa J.M., Renaud J., Muller B., Simonneau T., Genty B. 2013. The dual effect of abscisic acid on stomata. New Phytol. 197 : 65-72.
95. 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. 32 : 539-548.
96. Peto A., Lehotai N., Lozano-Juste J., León J., Tari I., Erdei L., Kolbert Z. 2011. Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann. Bot. 108 : 449-457.
97. Piotrowska-Niczyporuk A., Bajguz A., Zambrzycka E., Godlewska- Zylkiewicz B. 2012. Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol. Biochem. 52 : 52-65.
98. Poonam S., Kaur H., Geetika S. 2013. Effect of jasmonic acid on photosynthetic pigments and stress makers in Cajanus cajan (L.) Milsp. seedlings under copper stress. Amer. J. Plant Sci. 4 : 817-823.
99. Poschenrieder C., Gunsé B., Barceló J. 1989. Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol. 90 : 1365-1371.
100. Rady M.M. 2011. Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci. Horticult. 129 : 232-237.
101. Rady M.M., Osman A.S. 2012. Response of growth and antioxidant system of heavy metal-contaminated tomato plants to 24-epibrassinolide. Afr. J. Agric. Res. 7 : 3249-3254.
102. Rajewska I., Talarek M., Bajguz A. 2016. Brassinosteroids and Response of Plants to Heavy Metals Action. Front. Plant Sci. 7 : 1-5.
103. Ramakrishna B., Rao S.S.R. 2013. Preliminary studies on the involvement of glutathione metabolism and redox status against zinc toxicity in radish seedlings. Environ. Exp. Bot. 96 : 52-58.
104. Rauser W.E., Dumbroff E.B. 1981. Effects of excess cobalt, nickel and zinc on the water relations of Phaseolus vulgaris. Environ. Exp. Bot. 21 : 249-255.
105. Rodriguez-Serrano M., Romero-Puertas M.C., Pazmino D.M., Testillano P.S., Risueno M.C., del Rio L.A., Sandalio L.M. 2009. Cellular responses of pea plants to cadmium toxicity: Cross talk between ROS, Nitric oxide and calcium. Plant Physiol. 150 : 229-243.
106. Romanov G.A. 2009. How do cytokinins affect the cell? Russ. Plant Physiol. 56 : 268-290.
107. Rubio M.I., Escrig I., Martinez-Cortina C., Lopez-Benet F.J., Sanz A. 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.
108. Ruzicka K., Ljung K., Vanneste S., Podhorská R., Beeckman T.D., Friml J., Benková E. 2007. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 19 : 2197-2212.
109. Sah S.K., Reddy K.R., Li J. 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7 : 1-26.
110. Salt D.E., Prince R.C., Pickering I.J., Raskin I. 1995. Mechanisms of cadmium mobility and accumulation in Indian Mustard. Plant Physiol. 109 : 1427-1433.
111. Sauter A., Davies W.J., Hartung W. 2001. The long-distance abscisic acid signal in the droughted plant: The fate of the hormone on its way from root to shoot. J. Exp. Bot. 52 : 1991-1997.
112. Schat H., Sharma S.S., Vooijs R. 1997. Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol. Plant. 101 : 477-482.
113. Schellingen K., Straeten Van Der, Vandenbussche F., Prinsen E., Remans T. 2014. Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression. BMC Plant Biol. 14 : 214.
114. Schopfer P. 2001. Hydroxyl radical-induced cell wall loosening in vitro and in vivo: Implications for the control of elongation growth. Plant J. 28 : 679-688.
115. Shan X., Yan J., Xie D. 2012. Comparison of phytohormones signaling mechanisms. Curr. Opin. Plant Biol. 15 : 84-91.
116. Sharaf A.E.M.M., Farghal I.I,, Sofy M.R. 2009. Role of gibberellic acid in abolishing the detrimental effects of cadmium and lead on the broad bean and lupin plants. Res. J. Agric. Biol. Sci. 5 : 668-673.
117. Sharma I., Pati P.K., Bhardwaj R. 2011a. Effect of 24-epibrassinolide on oxidative stress markers induced by nickelion in Raphanus sativus L. Acta Physiol. Plant. 33 : 1723-1735.
118. Sharma I., Pati P.K., Bhardwaj R. 2011b. Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicol. 20 : 862-874.
119. Shi G.R., Cai Q.S., Liu Q.Q., Wu L. 2009. Salicylic acid-mediated alleviation of cadmium-toxicity in hemp plants in relation to cadmium uptake, photosynthesis and antioxidant enzymes. Acta Physiol. Plant. 31 : 969-977.
120. Shi W.G., Li H., Liu T.X., Polle A., Peng C.H., Luo Z.B. 2015. Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant Cell Environ. 38 : 207-223.
121. Shukla A., Srivastava S., Suprasanna P. 2017. Genomics of Metal Stress-Mediated Signalling and Plant Adaptive Responses in Reference to Phytohormones. Curr. 18 : 512-522.
122. Siddiqui M.H., Al-Whahibi M.H., Basalah M.O. 2011. Interactive effect of calcium and gibberellins on nickel tolerance in relation to antioxidant system in Triticum aestivum L. Protoplasma. 248 : 503-511.
123. Singh S., Prasad S.M. 2014. Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci. Horticult. 176. 1-10.
124. Singh A.P., Dixit G., Mishra S., Dwivedi S., Tiwari M., Mallick S., Pandey V., Trivedi P.K., Chakrabarty D., Tripathi R.D. 2015. Salicylic acid modulates arsenic toxicity by reducing its root to shoot translocation in rice (Oryza sativa L.). Front. Plant Sci. 6 : 340.
125. Singh V.P., Kumar J., Singh M., Singh S., Prasad S.M., Dwivedi R., Singh M.P.V.V.B. 2016. Role of salicylic acid-seed priming in the regulation of Cr(VI) and UV-B toxicity in maize seedlings. Plant Growth Regul. 78 : 79-91.
126. Sirhindi G., Mir M.A., Sharma P., Gill S Singh, Kaur Harpreet, Mushtaq R. 2015. Modulatory role of jasmonic acid on photosynthesis pigments, antioxidants and stress makers of Glycine max L. under nickel stress. Physiol. Mol. Biol. Plant. 21 : 559-565.
127. Srivastava A.K., Venkatachalam P., Raghothama K.G., Sahi S.V. 2007. Identification of lead-regulated genes by suppression subtractive hybridization in the heavy metal accumulator Sesbania drummondii. Planta. 225 : 1353-1365.
128. Srivastava S., Srivastava A.K., Suprasanna P., D'Souza S.F. 2009. Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. J. Exp. Bot. 60 : 3419-3431.
129. Srivastava S., Chiappetta A., Beatrice M. 2013. Identification and profiling of arsenic stress-induced miRNAs in Brassica juncea. J. Exp. Bot. 64 : 303-315.
130. Steffens B. 2014. The role of ethylene and ROS in salinity, heavy metal, and flooding responses in rice. Front. Plant Sci. 5 : 685.
131. Stroinski A., Chadzinikolau T., Gizewska K., Zielezinska M. 2010. ABA or cadmium induced phytochelatin synthesis in potato tubers. Biol. Plant. 54 : 117-120.
132. Swarup R., Perry P., Hagenbeek D., Van Der Staeten, Beemster G.T.S., Sandberg G., Bhalerao R., Ljung K., Bennett M.J. 2007. Ethylene regulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 19 : 2186-2196.
133. Tada Y., Spoel S.H., Pajerowska-Mukhtar K., Mou Z., Song J., Wang C., Zuo J., Dong X. 2008. Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science. 321 : 952-956.
134. Tandon S.A., Kumar R., Parsana S. 2015. Auxin treatment of wetland and non-wetland plant species to enhance their phytoremediation efficiency to treat municipal wastewater. J. Sci. Ind. Res. 74 : 702-707.
135. Thomas J.C., Perron M., LaRosa P.C., Smigocki A.C. 2005. Cytokinin and the regulation of a tobacco metallothionein-like gene during copper stress. Physiol. Plant. 123 : 262-271.
136. Trinh N., Huang T., Chi W., Fu S., Chen C. 2014. Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol. Plant. 150 : 205-224.
137. Vardhini B.V. 2014. Brassinosteroids role for amino acids, peptides and amines modulation in stressed plants (A review). In: Plant Adaptation to Environmental Change: Significance of Amino Acids and their Derivatives. Wallingford : CAB International : 300-316.
138. Vassilev A., Lidon F., Scotti P., Da Graca M., Yordanov I. 2004. Cadmium-induced changes in chloroplast lipids and photosystem activities in barley plants. Biol. Plant. 48 : 153-156.
139. Vasyuk V.A., Voytenko L.V., Shcherbatiuk M.M., Kosakivska I.V. 2019. Effect of exogenous abscisic acid on seed germination and growth of winter wheat seedlings under zinc stress. J. Stress Physiol. Biochem. 15 : 68-78.
140. Vernay P., Gauthier-Moussard C., Hitmi A. 2007. Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere. 68 : 1563-1575.
141. Veselov D.S., Kudoyarova G.R., Kudryakova, N.V., Kusnetsov V.V. 2017. Role of cytokinins in stress resistance of plants. Russ. J. Plant Physiol. 64 (1) : 15-27.
142. Vishwakarma K., Upadhyay N., Kumar N., Yadav G., Singh J., Mishra R., Kumar V., Verma R., UpadhyayG., Pandey M., Sharma S. 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant sci. 28 : 161-173.
143. Vodnik D., Gaberscik A., Gogala N. 1999. Lead phototoxicity in Norway spruce: the effects of lead and zeatin-riboside on root respiratory potential. Phyton. 39 : 155-159.
144. Wang J., Chen J., Pan K. 2013. Effect of exogenous abscisic acid on the level of antioxidants in Atractylodesma crocephala Koidz under lead stress. Environ. Sci. Pollut. Res. 20 : 1441-1449.
145. Wang R., Wang J., Zhao L., Yang S., Song Y. 2014a. Impact of heavy metal stresses on the growth and auxin homeostasis of Arabidopsis seedlings. BioMetals. 28 : 123-132.
146. Wang Y., Wang Y., Kai W., Zhao B., Chen P., Sun L., Ji K., Li Q., Dai S., Sun Y., Ji K., Li Q., Dai S., Sun, Wang Y., Pei Y., Leng P. 2014b. Transcriptional regulation of abscisic acid signal core components during cucumber seed germination and under Cu2+, Zn2+, NaCl and simulated acid rain stresses. Plant Physiol. Biochem. 76 : 67-76.
147. Wilkinson S., Davies W.J. 2002. ABA-based chemical signalling: The co-ordination of responses to stress in plants. Plant Cell Environ. 25 : 195-210.
148. Wilkinson S., Davies, W.J. 2010. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 33 : 510-525.
149. Xia X., Wang Y., Zhou Y., Tao Y., Mao W., Shi K., Asami T., Chen Z., Yu J. 2009. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance. Plant Physiol. 150 : 801-814.
150. Xu Y-X., Mao J., Chen W., Qian T-T., Liu S-C., Hao W-J., Li C-F., Chen L. 2016. Identification and expression profiling of the auxin response factors (ARFs) in the tea plant (Camellia sinensis (L.) O. Kuntze) under various abiotic stresses. Plant Physiol. Biochem. 98 : 46-56.
151. Yeh C., Hung W., Huang H. 2003. Copper treatment activates mitogen-activated protein kinase signalling in rice. Physiol. Plant. 119 : 392-399.
152. Yeh C., Hsiao L., Huang H. 2004. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol. 45 : 1306-1312.
153. Yeh C.M., Chien P.S., Huang H.J. 2007. Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J. Exp. Bot. 58 : 659-671.
154. Yoon G.M., Kieber J.J. 2013. 1-Aminocyclopropane-1-carboxylic acid as a signalling molecule in plants. AoB Plants. 5 : plt017.
155. Yu L., Luo Y.F., Liao B., Xie L.J., Chen L., Xiao S., Li J., Hu S., Shu W. 2012. Comparative transcriptomics analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol. 195 : 97-112.
156. Yuan H., Huang X. 2016. Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ. 39 : 120-135.
157. Yusuf M., Fariduddin Q., Hayat S., Hasan S.A., Ahmad A. 2010. Protective response of 28-Homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Arch. Environ. Contam. Toxicol. 60 : 68-76.
158. Yusuf M., Fariduddin Q., Ahmad A. 2012. 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiate under different levels of nickel: A shotgun approach. Plant Physiol. Biochem. 57 : 143-153.
159. Zelinová V., Alemayehu A., Bocová B., Huttová J., Tamás L. 2015. Cadmium-induced reactive oxygen species generation, changes in morphogenic responses and activity of some enzymes in barley root tip are regulated by auxin. Biologia. 70 : 356-364.
160. Zhang Y., Zheng G.H., Liu P., Song J.M., Xu G.D., Cai M.Z. 2011. Morphological and physiological responses of root tip cells to Fe2+ toxicity in rice. Acta Physiol. Plant. 33 : 683-689.
161. Zhang F., Zhang H., Xia Y., Wang G., Xu L., Shen Z. 2011. Exogenous application of salicylic acid alleviates Cd-toxicity and reduces hydrogen peroxide accumulation in root apoplasts of Phaseolus aureus and Vicia sativa. Plant Cell Rep. 30 : 1475-1483.
162. Zhao H., Wu L., Chai T., Zhang Y., Tan J., Ma S. 2012. The effects of copper, manganese and zinc on plant growth and elemental accumulation in the manganese-hyperaccumulator Phytolacca americana. J. Plant Physiol. 169 : 1243-1252.
163. Zhu X.F., Jiang T., Wang Z.W., Lei G.J., Shi Y.Z., Li G.X., Zheng S.J. 2012. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J. Hazard. Mater. 239 : 302-307.
164. Zhu X.F., Wang Z.W., Dong F., Lei G.J., Shi Y.Z., Li G.X., Zheng S.J. 2013. Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J. Hazard. Mater. 263 : 398-403.