Вісн. Харків. нац. аграрн. ун-ту. Сер. Біологія, 2018, вип. 3 (45), с. 10-30


https://doi.org/10.35550/vbio2018.03.010




РОСЛИНИ І ВАЖКІ МЕТАЛИ: РЕЦЕПЦІЯ ТА СИГНАЛІНГ


Н. О. Білявська, О. М. Федюк, О. К. Золотарьова

Інститут ботаніки ім. М.Г. Холодного
Національної академії наук України
(Київ, Україна)
E-mail: nbel2@ukr.net


Важкі метали є природними компонентами земної кори, які накопичуються з геогенних і антропогенних джерел, що призводить до забруднення екосистем і до значних втрат продуктивності культурних і дикорослих рослин. Вивчення того, як рослини можуть трансформувати сигнали про постійні зміни у середовищі в фізіологічні реакції, важливе для зниження шкідливих ефектів важких металів. Огляд стосується функціонування систем рецепції та сиг-налінгу важких металів, що існують в рослинах. Вважається, що компонент сигнальної мережі при стресі, спричинюваному важкими металами, може включати в себе рецептори для сприйняття сигнальних і небілкових месенджерів, які використовуються для передачі сигналу. Ряд ферментів, включаючи мітогенактивовані протеїнкінази і фосфатази, ретранслюють сигнали і викликають експресію генів різних транскрипційних факторів. У відповідь на вплив важкого металу відбувається посилена генерація АФК, що порушує нормальне функціонування клітини і викликає окиснювальне пошкодження біомакромолекул. Недавні дослідження розширили уявлення про роль гормонів рослин в рецепції стресу важких металів. Останнім часом розглядається ряд нових учасників процесів рецепції і трансдукції стгналів важких металів.


Ключові слова:важкі метали, сигналізація, рецепція, Са2+ сигнали, мітогенактивовані протеїнкінази, АФК, гормони

 


ЛІТЕРАТУРА


1. Vodka M.V., Polischuk A.V., Belyavskaya N.A., Zolotareva E.K. 2013. Effect of heavy metals on the photosynthetic apparatus and the activity of carbonic anhydrase in pea chloroplasts. Bull. Kharkiv. Natl. Agrar. Univ. Ser. Biology. (Visnyk Kharkiv. Natsional. Agrarn. Univer. Ser. Biologiya). 1 (43) : 46-55.
 
2. Kolupaev Yu.Ye., Karpets Yu.V. Formation of plants adaptive reactions to abiotic stressors influence. (Formirovanie adaptvnykh reaktsii ratenii na daistvie abi-oticheskikh strssorov). Kiеv : 352 p.
 
3. Medvedev I.F., Derevyagin S.S. 2017. Heavy metals in ecosystems (Tyazhelye metally v ekosistemakh). Saratov : 178 p.
 
4. Nefyodova O. O., Kuznetsova O.V., Zadese-nets I.P., Halperin O.I. 2017. Analysis of bib-liographic data on the influence of heavy metals on the cardiovascular system. Bulle-tin of Biology and Medicine. (Visn. Probl. Biol. Med.). 1 (4) : 53-60.
 
5. Polishchuk A.V., Semenikhin A.V., Topchyi N.M., Zolotareva E.K. 2018. Inhibition of multiple forms of carbonic anhydrases of spinach chloroplasts by Cu ions. Dopovidi. Nat. acad. Sci. Ukr. 4 : 94-101.
https://doi.org/10.15407/dopovidi2018.04.094
 
6. Ahmad P., Sarwat M., Bhat N.A., Wani M.R., Kazi A.G., Tran L.S.P. 2015. Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application in-volves various physiological and biochemi-cal strategies. PLoS One. 10 (1). e0114571.
https://doi.org/10.1371/journal.pone.0114571
 
7. Ali S., Rizwan M., Ullah N., Bharwana S.A., Waseem M., Farooq M.A., Abbassi G.H., Fareed M. 2016. Physiological and biochemical mechanisms of silicon-induced copper stress tolerance in cotton (Gossypium hirsutum L.). Acta Physiol. Plant. 38 : 1-11.
https://doi.org/10.1007/s11738-016-2279-3
 
8. Andosch A., Höftberger M., Lütz C., Lütz-Meindl U. 2015. Subcellular Sequestration and impact of heavy metals on the ultra-structure and physiology of the multicellular freshwater alga Desmidium swartzii. Int. J. Mol. Sci. 16 : 10389-10410.
https://doi.org/10.3390/ijms160510389
 
9. Anjum N.A., Aref I.M., Duarte A.C., Pereira, E., Ahmad I., Iqbal M. 2014. Glutathione and proline can coordinately make plants with-stand the joint attack of metal(loid) and sa-linity stresses. Front. Plant Sci. 5 : 662.
https://doi.org/10.3389/fpls.2014.00662
 
10. Arena C., Figlioli F., Sorrentino M.C., Izzo L.G., Capozzi F., Giordano S., Spagnuolo V. 2017. Ultrastructural, protein and photosyn-thetic alterations induced by Pb and Cd in Cynara cardunculus L., and its potential for phytoremediation. Ecotoxicol. Environ. Saf. 145 : 83-89.
https://doi.org/10.1016/j.ecoenv.2017.07.015
 
11. Asano T., Hayashi N., Kobayashi M., Aoki N. 2012. A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J. 69: 26-36.
https://doi.org/10.1111/j.1365-313X.2011.04766.x
 
12. Balasaraswathi K., Jayaveni S., Sridevi J., Sujatha D., Aaron K. P., Rose C. 2017. Cr-induced cellular injury and necrosis in Gly-cine max L.: Biochemical mechanism of oxi-dative damage in chloroplast. Plant Physiol. Biochem. 118 : 653-666.
https://doi.org/10.1016/j.plaphy.2017.08.001
 
13. Baliardini C., Meyer C.-L., Salis P., Saumitou-Laprade P., Verbruggen N. 2015. CATION EXCHANGER1 cosegregates with cadmium tolerance in the metal hyperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis Spp. Plant Physiol. 169 : 549-559.
https://doi.org/10.1104/pp.15.01037
 
14. Barrameda-Medina Y., Montesinos-Pereira D., Romero L 2014. Role of GSH homeostasis under Zn toxicity in plants with different Zn tolerance. Plant Sci. 227 : 110-121.
https://doi.org/10.1016/j.plantsci.2014.07.010
 
15. Bartels S., Gonźalez Besteiro M.A., Lang D., Ulm R. 2010. Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci. 15 : 322-329.
https://doi.org/10.1016/j.tplants.2010.04.003
 
16. Bashir K., Rasheed S., Kobayashi T., Seki M., Nishizawa N.K. 2016. Regulating Sub-cellular Metal Homeostasis: The Key to Crop Improvement. Front. Plant Sci. 7 : 1192.
https://doi.org/10.3389/fpls.2016.01192
 
17. Bickerton P. D., Pittman J. K. 2015. Role of cation/proton exchangers in abiotic stress signaling and stress tolerance in plants. In: Elucidation of Abiotic Stress Signaling in Plants. Springer : 95-117.
https://doi.org/10.1007/978-1-4939-2211-6_4
 
18. Bigeard J., Hirt H. 2018. Nuclear Signaling of Plant MAPKs. Front. Plant Sci. 9 : 469.
https://doi.org/10.3389/fpls.2018.00469
 
19. Bücker-Neto L., Paiva A.L.S., Machado R.D., Arenhar R.A., Margis-Pinheiro M. 2017. In-teractions between plant hormones and heavy metals responses.Gen. Mol. Biol. 40 (1) : 373-386.
https://doi.org/10.1590/1678-4685-gmb-2016-0087
 
20. Chandrasekhar C., Ray J. G. 2017. Copper accumulation, localization and antioxidant response in Eclipta alba L. in relation to quantitative variation of the metal in soil. Acta Physiol. Plant. 39 (9) : 205.
https://doi.org/10.1007/s11738-017-2508-4
 
21. Charabi Y., Choudri B. S., Ahmed M. 2018. Ecological and human health risk assess-ment. Water Environ. Res. 90 (10) : 1777-1791.
https://doi.org/10.2175/106143018X15289915807434
 
22. Chen L., Hu W., Tan S., Wang M. 2012. Ge-nome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. Plos One. 7 (10) : e46774.
https://doi.org/10.1371/journal.pone.0046744
 
23. Chen Y.A., Chi W.C., Trinh N.N., Huang L.Y. 2014. Transcriptome profiling and physio-logical studies reveal a major role for aro-matic amino acids in mercury stress toler-ance in rice seedlings. PloS One. 9 : e95163.
https://doi.org/10.1371/journal.pone.0095163
 
24. Cheng S., Tam N. F. Y., Li R., Shen X., Niu Z., Chai M., Qiu G. Y. 2017. Temporal varia-tions in physiological responses of Kandelia obovata seedlings exposed to multiple heavy metals. Marine Pollut. Bull. 124 (2) : 1089-1095.
https://doi.org/10.1016/j.marpolbul.2017.03.060
 
25. Chmielowska-Bak J., Izbianska K., Deckert J. 2015. Products of lipid, protein and RNA oxidation as signals and regulators of gene expression in plants. Front. Plant Sci. 6 : 405.
https://doi.org/10.3389/fpls.2015.00405
 
26. Chmielowska-Bak J., Izbianska K., Ekner-Grzyb A., Bayar M., Deckert J. 2018. Cad-mium stress leads to rapid increase in RNA oxidative modifications in soybean seed-lings. Front. Plant Sci. 8 : 2219.
https://doi.org/10.3389/fpls.2017.02219
 
27. Cho S-C., Chao Y-Y., Kao C.H. 2012. Calci-um deficiency increases Cd toxicity and Ca is required for heat-shock induced Cd toler-ance in rice seedlings. J. Plant Physiol. 169 (9) : 892-898.
https://doi.org/10.1016/j.jplph.2012.02.005
 
28. Conde A., Chaves M.M., Geros H. 2011. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52 : 1583-1602.
https://doi.org/10.1093/pcp/pcr107
 
29. Cuypers A., Keunen E., Bohler S., Jozefczak M., Opdenakker K., Gielen H. 2012. Cadmi-um and copper stress induce a cellular oxi-dative challenge leading to damage versus signaling. In: Metal Toxicity in Plants: Per-ception, Signaling and Remediation. Berlin, Heidelberg. Springer : 65-90.
https://doi.org/10.1007/978-3-642-22081-4_4
 
30. Czarnocka W., Karpinski S. 2018. Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic. Biol. Med. 122 : 4-20.
https://doi.org/10.1016/j.freeradbiomed.2018.01.011
 
31. Das K., Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of anti-oxidants as ROS-scavengers during envi-ronmental stress in plants. Front. Environ. Sci. 2 : 53.
https://doi.org/10.3389/fenvs.2014.00053
 
32. de la Torre F., Gutiérrez-Beltrán E., Pareja-Jaime Y., Chakravarthy S., Martin G. B., del Pozo O. 2013. The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. Plant Cell. 25 : 2748-2764.
https://doi.org/10.1105/tpc.113.113530
 
33. del Río L. A. 2015. ROS and RNS in plant physiology: an overview. J. Exp. Bot. 66 : 2827-2837.
https://doi.org/10.1093/jxb/erv099
 
34. Demidchik V. 2015. Mechanisms of oxida-tive stress in plants: from classical chemistry to cell biology. Environ. Exp. Bot. 109 : 212-228.
https://doi.org/10.1016/j.envexpbot.2014.06.021
 
35. Demidchik V., Maathuis F., Voitsekhovskaja O. 2018. Unravelling the plant signalling machinery: an update on the cellular and ge-netic basis of plant signal transduction. Funct. Plant Biol. 45 (2) : 1-8.
https://doi.org/10.1071/FP17085
 
36. DiMario R. J., Clayton H., Mukherjee A., Ludwig M., Moroney J.V. 2017. Plant car-bonic anhydrases: structures, locations, evo-lution, and physiological roles. Mol. Plant. 10 : 30-46.
https://doi.org/10.1016/j.molp.2016.09.001
 
37. Dóczi R., Ökrész L., Romero A.E., Paccanaro A., Bögre L. 2012. Exploring the evolution-ary path of plant MAPK networks. Trends Plant Sci. 17 : 518-525.
https://doi.org/10.1016/j.tplants.2012.05.009
 
38. Dodd A.N., Kudla J., Sanders D. 2010. The language of calcium signaling. Annu. Rev. Plant. Biol. 61 : 593-620.
https://doi.org/10.1146/annurev-arplant-070109-104628
 
39. Druege U., Franken P., Hajirezaei M. R. 2016. Plant hormone homeostasis, signaling, and function during adventitious root for-mation in cuttings. Front. Plant Sci. 7 : 381.
https://doi.org/10.3389/fpls.2016.00381
 
40. Dubey S., Shri M., Gupta A., Rani V., Chakrabarty D. 2018. Toxicity and detoxifi-cation of heavy metals during plant growth and metabolism. Environ. Chem. Lett. 1-24.
https://doi.org/10.1007/s10311-018-0741-8
 
41. Dubey S., Misra P., Dwivedi S., Chatterjee S., Bag S.K., Mantri S., Asif M.H., Rai A., Kumar S., Shri M., Tripathi P., Tripathi R.D., Trivedi P.K., Chakrabarty D., Tuli R. 2010. Tran-scriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Ge-nomics. 11 (1) : 648.
https://doi.org/10.1186/1471-2164-11-648
 
42. Dubey S., Shri M., Misra P., Lakhwani D., Bag S.K., Asif M.H., Trivedi P.K., Tripathi R.D., Chakra¬barty D. 2014. Heavy metals in-duce oxidative stress and genome-wide modulation in transcriptome of rice root. Funct. Integr. Genomics 14, 401-417.
https://doi.org/10.1007/s10142-014-0361-8
 
43. Edel K.H., Kudla J. 2015. Increasing com-plexity and versatility: how the calcium sig-naling toolkit was shaped during plant land colonization. Cell Calcium. 57 (3) : 231-246.
https://doi.org/10.1016/j.ceca.2014.10.013
 
44. Emamverdian A., Ding Y., Mokhberdoran F., Xie Y. 2015. Heavy metal stress and some mechanisms of plant defense response. Sci. World J. : 1-18. Article ID 756120.
https://doi.org/10.1155/2015/756120
 
45. Fang H., Jing T., Liu Z., Zhang L., Jin Z., Pei Y. 2014. Hydrogen sulfide interacts with cal-cium signaling to enhance the chromium tol-erance in Setaria italic. Cell Calcium. 56, 472-481.
https://doi.org/10.1016/j.ceca.2014.10.004
 
46. Fariduddin Q., Khalil R.R., Mir B.A., Yusuf M., Ahmad A. 2013. 24-Epibrassinolide reg-ulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sa-tivus under salt and/or copper stress. Envi-ron. Monit. Assess. 185 : 7845-7856.
https://doi.org/10.1007/s10661-013-3139-x
 
47. Fariduddin Q., Yusuf M., Ahmad I., Ahmad A. 2014. Brassinosteroids and their role in response of plants to abiotic stresses. Biol. Plant. 58 : 9-17.
https://doi.org/10.1007/s10535-013-0374-5
 
48. Farnese F.S., Menezes-Silva P.E., Gusman G.S., Oliveira J.A. 2016. When Bad Guys Become Good Ones: The Key Role of Reac-tive Oxygen Species and Nitric Oxide in the Plant Responses to Abiotic Stress. Front. Plant Sci. 7 : 471.
https://doi.org/10.3389/fpls.2016.00471
 
49. Farooq H., Asghar H.N., Khan M.Y., Saleem M., Zahir Z.A. 2015. Auxin-mediated growth of rice in cadmium-contaminated soil. Turk. J. Agric. For. 39 : 272-276.
https://doi.org/10.3906/tar-1405-54
 
50. Fonia A., Singh P., Singh V., Kumar D., Tripathi B.N. 2018. Molecular mechanisms of heavy metal hyperaccumulation in plants. In: Phytoremediation of Environmental Pol-lutants. CRC Press : 99-116.
 
51. Foyer C.H. 2018. Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ. Exp. Bot. 154 : 134-142.
https://doi.org/10.1016/j.envexpbot.2018.05.003
 
52. Foyer C.H., Noctor G. 2013. Redox signaling in plants. Antioxid. Redox Signal. 18 : 2087-2090.
https://doi.org/10.1089/ars.2013.5278
 
53. Galal T. M., Gharib F. A., Ghazi S. M., Mansour K. H. 2017. Metal uptake capabil-ity of Cyperus articulatus L. and its role in mitigating heavy metals from contaminated wetlands. Environ. Sci. Pollut. Res. 24 (27) : 21636-21648.
https://doi.org/10.1007/s11356-017-9793-8
 
54. Georgiadou E. C., Kowalska E., Patla K., Kulbat K., Smolinska B., Leszczynska J., Fotopoulos V. 2018. Influence of heavy metals (Ni, Cu and Zn) on nitro-oxidative stress responses, proteome regulation and al-lergen production in basil (Ocimum basili-cum L.) plants. Front. Plant Sci. 9 : 862.
https://doi.org/10.3389/fpls.2018.00862
 
55. Gill M. 2014. Heavy metal stress in plants: a review. Int. J. Adv. Res. 2 (6) : 1043-1055.
 
56. Gilroy S., Białasek M., Suzuki N., Górecka M., Devireddy A. R., Karpiński S., Mittler R. 2016. ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171 : 1606-1615.
https://doi.org/10.1104/pp.16.00434
 
57. Gonzalez A., Cabrera M.L., Henriquez M.J., Contreras R.A., Morales B., Moenne A. 2012. Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol. 15 : 1451-1462.
https://doi.org/10.1104/pp.111.191759
 
58. González-Fontes A., Navarro-Gochicoa M.T., Ceacero C.J., Herrera-Rodríguez M.B., Camacho-Cristóbal J.J., Rexach J. 2018. Un-derstanding calcium transport and signaling, and its use efficiency in vascular plants. In: Plant Macronutrient Use Efficiency. Aca-demic Press : 166-180.
https://doi.org/10.1016/B978-0-12-811308-0.00009-0
 
59. Goswami S., Das S. 2015. A study on cadmi-um phytoremediation potential of Indian mustard, Brassica juncea. Int. J. Phytoremed. 17 (6) : 583-588.
https://doi.org/10.1080/15226514.2014.935289
 
60. Goswami S., Kumar R.R., Sharma S.K., Kala Y.K., Singh K., Gupta R., Dhavan G., Rai G.K., Singh G.P., Pathak H., Rai R.D. 2015. Calcium triggers protein kinases-induced signal transduction for augmenting the ther-motolerance of developing wheat (Triticum aestivum) grain under the heat stress. J. Plant Biochem. Biotechnol. 24 : 441-452.
https://doi.org/10.1007/s13562-014-0295-1
 
61. Greeff C., Roux M., Mundy J., Petersen M. 2012. Receptor-like kinase complexes in plant innate immunity. Front. Plant Sci. 3 (4) : 264-270.
https://doi.org/10.3389/fpls.2012.00209
 
62. Guan C., Ji J., Jia C., Guan, W., Li X., Jin C., Wang G. 2015. A GSHS-like gene from Lycium chinense may be regulated by cadmium-induced endogenous salicylic acid and overexpression of this gene enhances tolerance to cadmium stress in Arabidopsis. Plant Cell Rep. 34 : 871-884.
https://doi.org/10.1007/s00299-015-1750-8
 
63. Hac-Wydro K., Sroka A., Jablo K. 2016. The impact of auxins used in assisted phytoex-traction of metals from the contaminated en-vironment on thea alterations caused by lead (II) ions in the organization of model lipid membranes. Colloids Surfaces B Biointer-faces 143 : 124-130.
https://doi.org/10.1016/j.colsurfb.2016.03.018
 
64. Hameed A., Rasool S., Azooz M. M., Hossain M. A., Ahanger M. A., Parvaiz A. 2016. Heavy metal stress: plant responses and sig-naling. In: Plant Metal Interaction. Elsevier : 557-583.
https://doi.org/10.1016/B978-0-12-803158-2.00024-2
 
65. Hamel L. P., Sheen J., Séguin A. 2014. An-cient signals: comparative genomics of green plant CDPKs. Trends Plant Sci. 19 : 79-89.
https://doi.org/10.1016/j.tplants.2013.10.009
 
66. Han Y., Wang S., Zhao N., Deng S., Zhao C., Li N., Chen S. 2016. Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd2+ influx in Populus euphratica cells. J. Plant Growth Regul. 35 : 827-837.
https://doi.org/10.1007/s00344-016-9585-2
 
67. Hasan S.A., Hayat S., Ahmad A. 2011. Brassinosteroids protect photosynthetic ma-chinery against the cadmium-induced oxida-tive stress in two tomato cultivars. Chemo-sphere. 84 : 1446-1451.
https://doi.org/10.1016/j.chemosphere.2011.04.047
 
68. Hashimoto K., Kudla J. 2011. Calcium de-coding mechanisms in plants. Biochimie. 93 (12) : 2054-2059.
https://doi.org/10.1016/j.biochi.2011.05.019
 
69. Hassan Z., Ali S., Ahmad R., Rizwan M., Ab-bas F., Yasmeen T., Iqbal M. 2017. Biochem-ical and molecular responses of oilseed crops to heavy metal stress. In: Oilseed Crops: Yield and Adaptations under Envi-ronmental Stress. John Wiley & Sons : 236-248.
https://doi.org/10.1002/9781119048800.ch13
 
70. Hassinen V. H., Tervahauta A. I., Schat H., Ka S. O. 2011. Plant metallothioneins - met-al chelators with ROS scavenging activity? Plant Biol. 13 : 225-232.
https://doi.org/10.1111/j.1438-8677.2010.00398.x
 
71. Hayat S. 2012. Foliar spray of brassinoster-oid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J. Biol. Sci. 19 : 325-335.
https://doi.org/10.1016/j.sjbs.2012.03.005
 
72. Himschoot E., Beeckman T., Friml J., Van-neste S. 2015. Calcium is an organizer of cell polarity in plants. BBA Molecular Cell Re-search. 1853 (9) : 2168-2172.
https://doi.org/10.1016/j.bbamcr.2015.02.017
 
73. Hu W., Lv Y., Lei W., Li X., Chen Y.H., Zheng L.Q., Xia Y., Shen Z.G. 2014. Cloning and characterization of the Oryza sativa wall-associated kinase gene OsWAK11 and its transcriptional response to abiotic stresses. Plant Soil. 384 : 335-346.
https://doi.org/10.1007/s11104-014-2204-8
 
74. Hu Y.F., Zhou G., Na X.F., Yang L., Nan W.B., Liu X. 2013. Cadmium interferes with maintenance of auxin homeostasis in Ara-bidopsis seedlings. J. Plant Physiol. 170 : 965-975.
https://doi.org/10.1016/j.jplph.2013.02.008
 
75. Huang D., Gong X., Liu Y., Zeng G., Lai C., Bashir H., Wan J. 2017. Effects of calcium at toxic concentrations of cadmium in plants. Planta. 245 : 863-873.
https://doi.org/10.1007/s00425-017-2664-1
 
76. Huang T.L., Nguyen Q.T.T., Fu S.F., Lin C.Y., Chen Y.C., Huang H.J. 2012. Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol. Biol. 80 : 587-608.
https://doi.org/10.1007/s11103-012-9969-z
 
77. Huang T.L., Huang L.Y., Fu S.F., Trinh N.N., Huang H.J. 2014. Genomic profiling of rice roots with short- and long- term chromium stress. Plant Mol. Biol. 86 : 157-170.
https://doi.org/10.1007/s11103-014-0219-4
 
78. Islam E., Khan M.T., Irem S. 2015. Biochem-ical mechanisms of signaling: perspectives in plant under arsenic stress. Ecotoxicol. Environ. Saf. 114 : 126-133.
https://doi.org/10.1016/j.ecoenv.2015.01.017
 
79. Jalmi S. K., Bhagat P. K., Verma D., Noryang S., Tayyeba S., Singh K., Sharma D., Sinha A. K. 2018. Traversing the Links between Heavy Metal Stress and Plant Signaling. Front. Plant Sci. 9 : 12.
https://doi.org/10.3389/fpls.2018.00012
 
80. Jalmi S. K., Sinha A. K. 2015. ROS mediated MAPK signaling in abiotic and biotic stress-striking similarities and differences. Front. Plant Sci. 6 : 769.
https://doi.org/10.3389/fpls.2015.00769
 
81. Jan S., Parray J. A. 2017. Heavy metal stress signalling in plants. In: Approaches to Heavy Metal Tolerance in Plants. Springer : 33-55.
https://doi.org/10.1007/978-981-10-1693-6_3
 
82. Janitza P., Ullrich K.K., Quint M. 2012. To-ward a comprehensive phylogenetic recon-struction of the evolutionary history of mi-togen-activated protein kinases in the plant kingdom. Front. Plant Sci. 3 : 271.
https://doi.org/10.3389/fpls.2012.00271
 
83. Jaskulak M., Rorat A., Grobelak A., Kacpr-zak M. 2018. Antioxidative enzymes and expression of rbcL gene as tools to monitor heavy metal-related stress in plants. J. Envi-ron. Manag. 218 : 71-78.
https://doi.org/10.1016/j.jenvman.2018.04.052
 
84. Jozefczak M., Remans T., Vangronsveld J., Cuypers A. 2012. Glutathione is a key player in metal-induced oxidative stress defenses. Int. J. Mol. Sci. 13 : 3145-3175.
https://doi.org/10.3390/ijms13033145
 
85. Kabir A.H. 2016. Biochemical and molecular changes in rice seedlings (Oryza sativa L.) to cope with chromium stress. Plant Biol. 18 : 710-719.
https://doi.org/10.1111/plb.12436
 
86. Kanojia A., Dijkwel P. P. 2018. Abiotic stress responses are governed by reactive oxygen species and age. Annu. Plant Rev. 1 : 1-32.
https://doi.org/10.1002/9781119312994.apr0611
 
87. Kanwar M.K., Bhardwaj R., Chowdhary S.P., Arora P., Sharma P., Kumar S. 2013. Isola-tion and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxi-dant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol. Plant. 35 : 1351-1362.
https://doi.org/10.1007/s11738-012-1175-8
 
88. Kanwar M.K., Poonam B.R. 2015. Arsenic induced modulation of antioxidative defense system and brassinosteroids in Brassica juncea L. Ecotoxicol. Environ. Saf. 115 : 119-125.
https://doi.org/10.1016/j.ecoenv.2015.02.016
 
89. Kapoor D., Rattan A., Gautam V., Kapoor N., Bhard¬waj R., Kapoor D., Rattan A., Gautam V., Kapoor N. 2014. 24-Epibrassinolide me-diated changes in photosynthetic pigments and antioxidative defence system of radish seedlings under cadmium and mercury stress. J. Stress Physiol. Biochem. 10 (3) : 110-121.
 
90. Kapoor D., Sharma R., Handa N., Kaur H., Rattan A., Yadav P., Gautam V., Kaur R., Bhardwaj R. 2015. Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front. Environ. Sci. 3 : 13.
https://doi.org/10.3389/fenvs.2015.00013
 
91. Karuppanapandian T., Moon J.C., Kim C., Manoharan K., Kim W. 2011. Reactive oxy-gen species in plants: their generation, signal transduction, and scavenging mechanisms. Austr. J. Crop Sci. 5 (6) : 709-725.
 
92. Kazan K. 2015. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 20 : 219-229.
https://doi.org/10.1016/j.tplants.2015.02.001
 
93. Khalil R.R., Moustafa A.N., Bassuony F.M., Haroun S.A. 2017. Kinetin and/or calcium affect growth of Phaseolus vulgaris L. plant grown under heavy metals stress. J. Environ. Sci. 46 (2) : 103-120.
 
94. Khan M., Daud M.K., Basharat A., Khan M.J., Azizullah A., Muhammad N., Muhammad N., Rehman Z., Zhu S.J. 2016а. Alleviation of lead-induced physiological, metabolic, and ultramorphological changes in leaves of upland cotton through glutathione. Environ. Sci. Pollut. Res. 23 (9) : 8431-8440.
https://doi.org/10.1007/s11356-015-5959-4
 
95. Khan M.I.R., Khan N.A., Masood A., Per T.S., Asgher M. 2016b. Hydrogen peroxide alle-viates nickel-inhibited photosynthetic re-sponses through increase in use-efficiency of nitrogen and sulfur, and glutathione pro-duction in mustard. Front. Plant Sci. 7 : 44.
https://doi.org/10.3389/fpls.2016.00044
 
96. Khan M.I.R., Nazir F., Asgher M., Per, T.S., Khan, N.A. 2015. 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.
https://doi.org/10.1016/j.jplph.2014.09.011
 
97. Kim T.W., Michniewicz M., Bergmann D.C., Wang Z.Y. 2012. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 482 : 419-422.
https://doi.org/10.1038/nature10794
 
98. Kim Y.H., Khan A. L., Kim D.H., Lee S.Y., Kim K.M., Waqas M., Lee I.J. 2014. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohor-mones. BMC Plant Biol.14 (1) : 13.
https://doi.org/10.1186/1471-2229-14-13
 
99. Kohli S.K., Handa N., Gautam V., Bali S., Sharma A., Khanna K., Arora S., Thukral A. K., Ohri P., Karpets Y.V., Kolupaev, Y.E., Bhardwaj R. 2017. ROS signaling in plants under heavy metal stress. In: Reactive Oxy-gen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress. Springer, Singapore : 185-214.
https://doi.org/10.1007/978-981-10-5254-5_8
 
100. Kolbert Z., Petö A., Lehotai N., Feigl G. Erdei L. 2012. Long-term copper (Cu) exposure impacts on auxin, nitric oxide (NO) metabolism and morphology of Arabidopsis thaliana L. Plant Growth Regul. 68 : 151-159.
https://doi.org/10.1007/s10725-012-9701-7
 
101. Komis G., Šamajová O., Ovečka M., Šamaj J. 2018. Cell and developmental biol-ogy of plant mitogen-activated protein ki-nases. Annu. Rev. Plant. Biol. 69 : 237-265.
https://doi.org/10.1146/annurev-arplant-042817-040314
 
102. Krishnamurthy A., Rathinasabapathi B. 2013. Auxin and its transport play a role in plant tolerance to arsenite-induced oxida-tive stress in Arabidopsis thaliana. Plant Cell Environ. 36 : 1838-1849.
https://doi.org/10.1111/pce.12093
 
103. Kumar S., Asif M.H., Chakrabarty D., Tripathi R.D., Dubey R.S., Trivedi P.K. 2013. Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Ara-bidopsis provides tolerance to heavy metal and other abiotic stresses. J. Hazard Mat. 24 : 228-237.
https://doi.org/10.1016/j.jhazmat.2013.01.004
 
104. Kumar S., Dubey R.S., Tripathi R.D., Chakrabarty D., Trivedi P.K. 2015a. Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ. Int. 74 : 221-230.
https://doi.org/10.1016/j.envint.2014.10.019
 
105. Kumar S., Asif M.H., Chakrabarty D., Tripathi R.D., Dubey R.S., Trivedi P.K. 2015b. Comprehensive analysis of regulato-ry elements of the promoters of rice sulphate transporter gene family and functional char-acterisation of OsSul1;1 promoter under dif-ferent metal stress. Plant Signal. Behav. 10 (4) : e990843.
https://doi.org/10.4161/15592324.2014.990843
 
106. Kumar S., Trivedi P. K. 2016. Heavy metal stress signaling in plants. In: Plant Metal Interaction. Elsevier : 585-603.
https://doi.org/10.1016/B978-0-12-803158-2.00025-4
 
107. Lange B., Ent A., Baker A. J. M., Echevarria G., Mahy G., Malaisse F.,. Meerts P, Pourret O., Verbruggen N., Faucon M. P. 2017. Copper and cobalt accumulation in plants: a critical assessment of the current state of knowledge. New Phytol. 213 : 537-551.
https://doi.org/10.1111/nph.14175
 
108. Le Martret B., Poage M., Shiel K., Nugent G.D., Dix P.J. 2011. Tobacco chloro-plast transformants expressing genes encod-ing dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Bio-tech. J. 9 : 661-673.
https://doi.org/10.1111/j.1467-7652.2011.00611.x
 
109. Lee Y., KimY.J., Kim M.H., Kwak J.M. 2016. MAPK cascades in guard cell sig-nal transduction. Front. Plant Sci. 7 : 80.
https://doi.org/10.3389/fpls.2016.00080
 
110. 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.
https://doi.org/10.1016/j.plaphy.2010.05.005
 
111. Levine B.A., Williams R.J.P. 1982. Calcium binding to proteins and other large biological anion centers. In: Calcium and Cell Function. New York, Acad. Press : 1-38.
https://doi.org/10.1016/B978-0-12-171402-4.50007-1
 
112. Li Z., Xing D. 2010. Mitochondrial pathway leading to programmed cell death induced by aluminum phytotoxicty in Ara-bidopsis. Plant Signal Behav. 5 : 1660-1662.
https://doi.org/10.4161/psb.5.12.14014
 
113. Li Z.Y., Xu Z.S., He G.Y., Yang G.X., Chen M., Li L.C., Ma Y.Z. 2012. Overexpres-sion of soybean GmCBL1 enhances abiotic stress tolerance and promotes hypocotyl elongation in Arabidopsis. Biochem. Bio-phys. Res. Commun. 427 : 731-736.
https://doi.org/10.1016/j.bbrc.2012.09.128
 
114. Li P., Zhao C. Z., Zhang Y. Q.,Wang X.M.,Wang X. Y.,Wang J. F. 2016. Calcium alleviates cadmium-induced inhibition on root growth bymaintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma. 253 : 185-200.
https://doi.org/10.1007/s00709-015-0810-9
 
115. Lim C.W., Yang S.H., Shin K.H., Lee S.C., Kim S.H. 2015. The AtLRK10L1.2, Arabidopsis, ortholog of wheat LRK10, is involved in ABA-mediated signaling and drought resistance. Plant Cell Rep. 34 : 447-455.
https://doi.org/10.1007/s00299-014-1724-2
 
116. Lin C.Y., Trinh N.N., Lin C.W., Huang H.J. 2013. Transcriptome analysis of phytohormone, transporters and signaling pathways in response to vanadium stress in rice roots. Plant Physiol. Biochem. 66 : 98-104.
https://doi.org/10.1016/j.plaphy.2013.02.007
 
117. Lionetto M.G., Caricato R., Giordano M.E., Schettino T. 2016.The com-plex relationship between metals and car-bonic anhydrase: new insights and perspec-tives. Int. J. Mol. Sci. 17 : E127.
https://doi.org/10.3390/ijms17010127
 
118. Liu W.J., Wood B.A., Raab A., McGrath S.P., Zhao F.J., Feldmann J. 2010. Complexation of arsenite with phytochela-tins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. Plant Physiol. 152 : 2211-2221.
https://doi.org/10.1104/pp.109.150862
 
119. Liu S., Yang R., Tripathi D.K., Li X., He W., Wu M., Pan Y. 2018. The interplay between reactive oxygen and nitrogen spe-cies contributes in the regulatory mechanism of the nitro-oxidative stress induced by cadmium in Arabidopsis. J. Hazard. Mater. 344 : 1007-1024.
https://doi.org/10.1016/j.jhazmat.2017.12.004
 
120. Luo Z.B., J. He, A. Polle, H. Ren-nenberg 2016. Heavy metal accumulation and signal transduction in herbaceous and woody plants: Paving the way for enhancing phytoremediation efficiency. Biotechnol. Adv. 34 : 1131-1148.
https://doi.org/10.1016/j.biotechadv.2016.07.003
 
121. Lushchak V. I. 2015. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem. Biol. Interact. 224 : 164-165.
https://doi.org/10.1016/j.cbi.2014.10.016
 
122. Ma Q., Grones P., Robert S. 2018. Auxin signaling: a big question to be ad-dressed by small molecules. J. Exp. Bot. 69 : 313-328.
https://doi.org/10.1093/jxb/erx375
 
123. Manohar M., Shigaki T., Hirschi K.D. 2011. Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol. 13 : 561-569.
https://doi.org/10.1111/j.1438-8677.2011.00466.x
 
124. Mansour S.A 2014. Heavy metals of special concern to human health and envi-ronment. In: Practical Food Safety: Contem-porary Issues and Future Directions. Wiley Blackwell : 213-233.
https://doi.org/10.1002/9781118474563.ch12
 
125. Marschner P. 2012. Marschner's Mineral Nutrition of Higher Plants. 3rd ed. New York. Academic Press.
 
126. Mhamdi A., Van Breusegem F. 2018. Reactive oxygen species in plant de-velopment. Development. 145 (15), dev164376.
https://doi.org/10.1242/dev.164376
 
127. Miransari M. 2012. Role of phyto-hormone signaling during stress. In: Envi-ronmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York : 381-393.
https://doi.org/10.1007/978-1-4614-0815-4_17
 
128. Mittler R. 2017. ROS Are Good. Trends Plant Sci. 22 : 11-19.
https://doi.org/10.1016/j.tplants.2016.08.002
 
129. Mohanta T.K., Kumar P., Bae H. 2017. Genomics and evolutionary aspect of calcium signaling event in calmodulin and calmodulin-like proteins in plants. BMC Plant Biol. 17 : 38.
https://doi.org/10.1186/s12870-017-0989-3
 
130. Montero-Palmero M.B., Martin-Barranco A., Escobar C., Hernandez L.E. 2014. Early transcriptional responses to mercury: a role for ethylene in mercury-induced stress. New Phytol. 201 : 116-130.
https://doi.org/10.1111/nph.12486
 
131. Mourato M. P., Moreira I. N., Leitão I., Pinto F. R., Sales J. R., Martins L. L. 2015. Effect of heavy metals in plants of the genus Brassica. Int. J. Mol. Sci. 16 : 17975-17998.
https://doi.org/10.3390/ijms160817975
 
132. Noctor G., Mhamdi A., Chaouch S., Han Y. I., Neukermans J., Marquez-Garcia B.E.L.E.N., Foyer C. H. 2012. Glutathione in plants: an integrated overview. Plant Cell Environ. 35 : 454-484.
https://doi.org/10.1111/j.1365-3040.2011.02400.x
 
133. Opdenakker K.; Remans T.; Keunen E.; Vangron¬sveld J.; Cuypers A. 2012. Ex-posure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated al-terations in MAPKinase transcript levels. Environ. Exp. Bot. 83 : 53-61.
https://doi.org/10.1016/j.envexpbot.2012.04.003
 
134. Pajević S., Borišev M., Nikolić N., Arsenov D. D., Orlović S., Župunski M. 2016. Phytoextraction of heavy metals by fast- growing trees: A review. In: Phytore-mediation. Springer : 23-64.
https://doi.org/10.1007/978-3-319-40148-5_2
 
135. Pandey C., Gupta M. 2015. Seleni-um and auxin mitigates arsenic stress in rice (Oryza sativa L.) by combining the role of stress indicators, modulators and genotoxici-ty assay. J. Hazard. Mat. 287 : 384-391.
https://doi.org/10.1016/j.jhazmat.2015.01.044
 
136. Paque S., Weijers D. 2016. Q&A: Auxin: the plant molecule that influences almost anything. BMC Biology 14 : 67.
https://doi.org/10.1186/s12915-016-0291-0
 
137. Per T.S., Khan S., Asgher M., Bano B., Khan N. A. 2016. Photosynthetic and growth responses of two mustard cultivars differing in phytocystatin activity under cadmium stress. Photosynthetica. 54 : 491-501.
https://doi.org/10.1007/s11099-016-0205-y
 
138. Perochon A., Aldon D., Galaud J. P., Ranty B. 2011. Calmodulin and calmodulin-like proteins in plant calcium signaling. Bio-chimie. 93 (12) : 2048-2053.
https://doi.org/10.1016/j.biochi.2011.07.012
 
139. Pittman J. K., Hirschi K. D. 2016. CAX-ing a wide net: Cation/H+ transporters in metal remediation and abiotic stress sig-nalling. Plant Biol. 18 : 741-749.
https://doi.org/10.1111/plb.12460
 
140. Rady M.M. 2011. Effect of 24-epibrassinolide on growth, yield, antioxidant systemand cadmiumcontent of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci. Horticult. 129 : 232-237.
https://doi.org/10.1016/j.scienta.2011.03.035
 
141. Rai A., Bhardwaj A., Misra P., Bag S.K., Adhikari B., Tripathi R.D., Chakrabarty D. 2015. Comparative transcriptional profiling of contrasting rice genotypes shows expression differences during arsenic stress. Plant Genome. 8 : 1-14.
https://doi.org/10.3835/plantgenome2014.09.0054
 
142. Rajewska I., Talarek M., Bajguz A. 2016. Brassinosteroids and Response of Plants to Heavy Metals Action. Front. Plant Sci. 7 : 629.
https://doi.org/10.3389/fpls.2016.00629
 
143. Ramakrishna B., Rao S.S.R. 2013. Preliminary studies on the involvement of glutathione metabolism and redox status against zinc toxicity in radish seedlings by 28-homobrassinolide. Environ. Exp. Bot. 96 : 52-58.
https://doi.org/10.1016/j.envexpbot.2013.08.003
 
144. Ranty B., Aldon D., Cotelle V., Ga-laud J. P., Thuleau P., Mazars C. 2016. Cal-cium sensors as key hubs in plant responses to biotic and abiotic stresses. Front. Plant Sci. 7 : 327.
https://doi.org/10.3389/fpls.2016.00327
 
145. Rao K.P., Vani G., Kumar K., Wank-hede D.P., Misra M., Gupta M., Sinha A.K. 2011. Arsenic stress activates MAP kinase in rice roots and leaves. Arch. Biochem. Bio-phys. 506 : 73-82.
https://doi.org/10.1016/j.abb.2010.11.006
 
146. Rao K.P., Richa T., Kuma K., Raghuram B., Sinha A.K. 2010. In silico analysis reveals 75 members of protein kinsase kinase kinase gene family in rice. DNA Res. 17 : 139-153.
https://doi.org/10.1093/dnares/dsq011
 
147. Rizwan M., Ali S., Adrees M., Rizvi H., Zia-ur-Rehman M., Hannan F., Ok Y. S. 2016. Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ. Sci. Pollut. Res. 23 : 17859-17879.
https://doi.org/10.1007/s11356-016-6436-4
 
148. Rodriguez-Hernandez M. C., Bonifas I., Alfaro-De la Torre M. C., Flores-Flores J. I., Bañuelos-Hernández B., Patiño-Rodríguez O. (2015). Increased accumulation of cadmium and lead under Ca and Fe deficiency in Typha latifolia: a case study of two pore channel (TPC1) gene. Environ. Exp. Bot. 115 : 38-48.
https://doi.org/10.1016/j.envexpbot.2015.02.009
 
149. Rout G.R., Panigrahi J. 2015. Analy-sis of signaling pathways during heavy metal toxicity: A functional genomics perspective. In: Elucidation of Abiotic Stress Signaling in Plants. Springer, New York : 295-322.
https://doi.org/10.1007/978-1-4939-2540-7_11
 
150. Sah S.K., Reddy K.R., Li J. 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7 : 571.
https://doi.org/10.3389/fpls.2016.00571
 
151. Samajova O., Plihal O., Al-Yousif M., Hirt H., Samaj J. 2013. Improvement of stress tolerance in plants by genetic manipu-lation of mitogen-activated protein kinases. Biotech. Adv. 31, 118-128.
https://doi.org/10.1016/j.biotechadv.2011.12.002
 
152. Schulz P., Herde M., Romeis T. 2013. Calcium-dependent protein kinases: hubs in plant stress signaling and develop-ment. Plant Physiol. 163 : 523-530.
https://doi.org/10.1104/pp.113.222539
 
153. Sethi V., Raghuram B., Sinha A. K., Chattopadhyay S. 2014. A mitogen-activated protein kinase cascade module, MKK3-MPK6 and MYC2, is involved in blue light-mediated seedling development in Ara-bidopsis. Plant Cell. l26 : 3343-3357.
https://doi.org/10.1105/tpc.114.128702
 
154. Sewelam N., Kazan K., Schenk P. M. 2016. Global plant stress signaling: reactive oxygen species at the cross-road. Front. Plant Sci. 7 : 187.
https://doi.org/10.3389/fpls.2016.00187
 
155. Sharma I., Pati P.K., Bhardwaj R. 2011. Effect of 24-epibrassinolide on oxida-tive stress markers induced by nickel ion in Raphanus sativus L. Acta Physiol. Plant. 33 : 1723-1735.
https://doi.org/10.1007/s11738-010-0709-1
 
156. Sharma P., Jha A.B., Dubey R.S., Pessarakli M. 2012. Reactive oxygen spe-cies, oxidative damage, and antoxidative de-fense mechanism in plants under stressful conditions. J. Bot. 2012 : 1-26.
https://doi.org/10.1155/2012/217037
 
157. Shukla D., Tiwari M., Tripathi R.D., Nath P., Trivedi P.K. 2013. Synthetic phyto-chelatins complement a phytochelatin-deficient Arabidopsis mutant and enhance the accumulation of heavy metal(loid)s. Bi-ochem. Biophys. Res. Commun. 434 : 664-669.
https://doi.org/10.1016/j.bbrc.2013.03.138
 
158. Siddiqui M.H., Al-Whaibi M.H., Sakran A.M., Basalah M.O., Ali H.M. 2012. Effect of calcium and potassium on antioxi-dant system of Vicia faba L. under cadmium stress. Int. J. Mol. Sci. 13 (6) : 6604-6619.
https://doi.org/10.3390/ijms13066604
 
159. Singh S., Parihar P., Singh R., Singh V. P., Prasad S. M. 2016. Heavy metal toler-ance in plants: role of transcriptomics, pro-teomics, metabolomics, and ionomics. Front. Plant Sci. 6 : 1143.
https://doi.org/10.3389/fpls.2015.01143
 
160. Singh I., Shah K. 2014. Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings. Phytochemistry. 108 : 57-66.
https://doi.org/10.1016/j.phytochem.2014.09.007
 
161. Sinha A. K., Jaggi M., Raghuram B., Tuteja N. 2011. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6 : 196-203.
https://doi.org/10.4161/psb.6.2.14701
 
162. Sirhindi G., Sharma P., Singh A., Kaur H., Mir M. 2015. Alteration in photo-synthetic pigments, osmolytes and antioxi-dants in imparting copper stress tolerance by exogenous jasmonic acid treatment in Ca-janus cajan. Int. J. Plant Physiol. Biochem. 7 (3) : 30-39.
 
163. Smeets K., Opdenakker K., Remans T., Forzani C., Hirt H., Vangronsveld J., Cuypers A. 2013. The role of the kinase OXI1 in cadmium- and copper-induced mo-lecular responses in Arabidopsis thaliana. Plant Cell Environ. 36 : 1228-1238.
https://doi.org/10.1111/pce.12056
 
164. Smékalová V., Doskočilová A., Ko-mis G., Šamaj J. 2014. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechn. Adv. 32 (1) : 2-11.
https://doi.org/10.1016/j.biotechadv.2013.07.009
 
165. Soni P., Nutan K. K., Soda N., Nong-piur R. C., Roy S., Singla-Pareek S. L., Pareek A. 2015. Towards understanding abiotic stress signaling in plants: convergence of genomic, transcriptomic, proteomic, and metabolomic approaches. In: Elucidation of Abiotic Stress Signaling in Plants. Springer, New York : 3-40.
https://doi.org/10.1007/978-1-4939-2211-6_1
 
166. Srivastava S., Srivastava A. K., Su-prasanna P., D'Souza S. F. 2013. Identifica-tion and profiling of arsenic stress-induced microRNAs in Brassica juncea. J. Exp. Bot. 64 : 303-315.
https://doi.org/10.1093/jxb/ers333
 
167. Steffens B. 2014. The role of eth-ylene and ROS in salinity, heavy metal, and flooding responses in rice. Front. Plant Sci. 5 : 685.
https://doi.org/10.3389/fpls.2014.00685
 
168. Steinhorst L., Kudla J. 2014. Signal-ing in cells and organisms - calcium holds the line. Curr. Opin. Plant Biol. 22 : 14-21.
https://doi.org/10.1016/j.pbi.2014.08.003
 
169. Stolpe C., Krämer U., Müller C. 2017. Heavy metal (hyper) accumulation in leaves of Arabidopsis halleri is accompa-nied by a reduced performance of herbi-vores and shifts in leaf glucosinolate and el-ement concentrations. Environ. Exp. Bot. 133 : 78-86.
https://doi.org/10.1016/j.envexpbot.2016.10.003
 
170. Straltsova D., Chykun P., Subramaniam S., Sosan A., Kolbanov D., Sokolik A. 2015. Cation channels are involved in brassinosteroid signalling in higher plants. Steroids 97 : 98-106.
https://doi.org/10.1016/j.steroids.2014.10.008
 
171. Su J., Xu J., Zhang S. 2015. RACK1, scaffolding a heterotrimeric G protein and a MAPK cascade. Trends Plant Sci. 20 : 405-407.
https://doi.org/10.1016/j.tplants.2015.05.002
 
172. Sun P., Tian Q.-Y., Chen J., Zhang W.-H. 2010. Aluminum-induced inhibition of root elongation in Arabidopsis is mediat-ed by ethylene and auxin. J. Exp. Bot. 61 : 347-356.
https://doi.org/10.1093/jxb/erp306
 
173. Sytar O., Kumar A., Latowski D., Kuczynska P., Strzalka K., Prasad M.N.V. 2013. Heavy metal-induced oxidative dam-age, defense reactions, and detoxification mechanisms in plants. Acta Physiol. Plant. 35 : 985-999.
https://doi.org/10.1007/s11738-012-1169-6
 
174. Taj G., Agarwal P., Grant M., Kumar A. 2010. MAPK machinery in plants: recog-nition and response to different stresses through multiple signal transduction path-ways. Plant Signal. Behav. 5 : 1370-1378.
https://doi.org/10.4161/psb.5.11.13020
 
175. Takahashi F., Mizoguchi T., Yo-shida R., Ichimura K., Shinozaki K. 2011. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell. 41 : 649-660.
https://doi.org/10.1016/j.molcel.2011.02.029
 
176. Takatsuka H, Umeda M. 2014. Hor-monal control of cell division and elonga-tion along differentiation trajectories in roots. J. Exp. Bot. 65 : 2633-2643.
https://doi.org/10.1093/jxb/ert485
 
177. Talukdar D. 2012. Exogenous calci-um alleviates the impact of cadmium-induced oxidative stress in Lens culinaris Medic. seedlings through modulation of an-tioxidant enzyme activities. J. Crop Sci. Bio-technol. 15 (4) : 325-334.
https://doi.org/10.1007/s12892-012-0065-3
 
178. Tamás L., Mistrík I., Zelinová V. 2017. Heavy metal-induced reactive oxygen species and cell death in barley root tip. Environ. Exp. Bot. 140 : 34-40.
https://doi.org/10.1016/j.envexpbot.2017.05.016
 
179. Tandon SA, Kumar R, Parsana S 2015. Auxin treatment of wetland and non-wetland plant species to enhance their phy-toremediation efficiency to treat municipal wastewater. J. Sci. Ind. Res. 74 : 702-707.
 
180. Thounaojam T.C., Panda P., Ma-zumdar P., Kumar D., Sharma GD., Sahoo L., Panda S.K. 2012. Excess copper induced ox-idative stress and response of antioxidants in rice. Plant Physiol. Biochem. 53 : 33-39.
https://doi.org/10.1016/j.plaphy.2012.01.006
 
181. Tiwari M., Sharma D., Singh M., Tripathi R.D., Trivedi P.K., 2014. Expression of OsMATE1 and OsMATE2 alters devel-opment, stress responses and pathogen sus-ceptibility in Arabidopsis. Sci. Rep. 4 : 1-12.
https://doi.org/10.1038/srep03964
 
182. Tran L., Pal S. 2014. Phytohor-mones: a window to metabolism, signaling, and biotechnological applications. Springer Science and Business Media New York : 161 p.
https://doi.org/10.1007/978-1-4939-0491-4
 
183. Trinh N.N., Huang T.L., Chi W.C., Fu S.F., Chen C.C., Huang H.Z. 2014. Chro-mium stress response effect on signal trans-duction and expression of signaling genes in rice. Physiol. Plant. 150 : 205-224.
https://doi.org/10.1111/ppl.12088
 
184. Venkataramaiah N., Ramakrishna S.V., Sreevathsa R. 2011. Overexpression of phytochelatin synthase (AtPCS) in rice for tolerance to cadmium stress. Biologia. 66 : 1060-1073.
https://doi.org/10.2478/s11756-011-0135-x
 
185. Verma V., Ravindran P., Kumar P.P. 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16 : 86.
https://doi.org/10.1186/s12870-016-0771-y
 
186. Villiers F., Jourdain A., Bastien O., Leonhardt N., Fujioka S., Tichtincky G. 2012. Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J. Exp. Bot. 63 : 1185-1200.
https://doi.org/10.1093/jxb/err335
 
187. Vishwakarma K., Upadhyay N., Kumar N., Yadav G., Singh J., Mishra R.K., Kumar V., Verma R., Upadhyay R.G., 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. 8 : 161.
https://doi.org/10.3389/fpls.2017.00161
 
188. Vitti A., Nuzzaci M., Scopa A., Tataranni G., Remans T., Vangronsveld J. 2013. Auxin and cytokinin metabolism and root morphological modifications in Ara-bidopsis thaliana seedlings infected with Cucumber mosaic virus (CMV) or exposed to cadmium. Int. J. Mol. Sci. 14 : 6889-6902.
https://doi.org/10.3390/ijms14046889
 
189. Wang P., Du Y., Li Y., Ren D., Song C.P. 2010. Hydrogen peroxide-mediated ac-tivation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell. 22 : 2981-2998.
https://doi.org/10.1105/tpc.109.072959
 
190. Wang W., Bai M.-Y., Wang Z.-Y. 2014. The brassinosteroid signaling network - a paradigm of signal integration. Curr. Opin. Plant Biol. 21 : 147-153.
https://doi.org/10.1016/j.pbi.2014.07.012
 
191. Wang R., Wang, J., Zhao L., Yang S., Song Y. 2015. Impact of heavy metal stress-es on the growth and auxin homeostasis of Arabidopsis seedlings. Biometals. 28 (1) : 123-132.
https://doi.org/10.1007/s10534-014-9808-6
 
192. Wang S., Ren X., Huang B., Wang G., Zhou P., An Y. 2016. Aluminium-induced reduction of plant growth in alfalfa (Medi-cago sativa) is mediated by interrupting auxin transport and accumulation in roots. Sci. Rep. 6 : 30079.
https://doi.org/10.1038/srep30079
 
193. Wang W., Bai M.-Y., Wang Z.-Y. 2014. The brassinosteroid signaling network - a paradigm of signal integration. Curr. Opin. Plant Biol. 21 : 147-153.
https://doi.org/10.1016/j.pbi.2014.07.012
 
194. Wang Y., Wang Y., Kai W., Zhao B., Chen P., Sun L., Wang, Y. 2014. Transcrip-tional regulation of abscisic acid signal core components during cucumber seed germina-tion and under Cu2+, Zn2+, NaCl and simulat-ed acid rain stresses. Plant Physiol. Biochem. 76 : 67-76.
https://doi.org/10.1016/j.plaphy.2014.01.003
 
195. Wang Y., Xu L., Chen Y., Shen H., Gong Y., Limera C., Liu L. 2013. Transcrip-tome profiling of radish (Raphanus sativus L.) root and identification of genes involved in response to lead (Pb) stress with next gen-eration sequencing. PLoS One. 8 (6) : e66539.
https://doi.org/10.1371/journal.pone.0066539
 
196. Wani S. H., Kuma, V., Shriram V., Sah S. K. 2016. Phytohormones and their metabolic engineering for abiotic stress tol-erance in crop plants. Crop J. 4 : 162-176.
https://doi.org/10.1016/j.cj.2016.01.010
 
197. Waszczak C., Carmody M., Kangasjärvi J. 2018. Reactive oxygen spe-cies in plant signaling. Annu. Rev. Plant Bi-ol. 69 : 209-236.
https://doi.org/10.1146/annurev-arplant-042817-040322
 
198. Wilkins K. A., Matthus E., Swarbreck S. M., Davies J. M. 2016. Calci-um-mediated abiotic stress signaling in roots. Front. Plant Sci. 7 : 1296.
https://doi.org/10.3389/fpls.2016.01296
 
199. Wu X., Cobbina S. J., Mao G., Xu H., Zhang Z., Yang L. 2016. A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ. Sci. Pollut. Res. 23 (9) : 8244-8259.
https://doi.org/10.1007/s11356-016-6333-x
 
200. Wu X., He J., Ding H., Zhu Z., Chen J., Xu S., Zha D. 2015. Modulation of zinc-induced oxidative damage in Solanum melongena by 6-benzylaminopurine involves ascorbate - glutathione cycle metabolism. Environ. Exp. Bot. 116 : 1-11.
https://doi.org/10.1016/j.envexpbot.2015.03.004
 
201. Wu Q., Shigaki, T., Williams K.A., Han J.S., Kim C.K., Hirschi K.D., Park S. 2011. Expression of an Arabidopsis Ca2+/H+ antiporter CAX1 variant in petunia enhances cadmium tolerance and accumulation. J. Plant Physiol. 168 : 167-173.
https://doi.org/10.1016/j.jplph.2010.06.005
 
202. Wu X.X., Chen J.L., Xu S., Zhu Z.W., Zha D.S. 2016. Exogenous 24-epibrassinolide alleviates zinc-induced tox-icity in eggplant (Solanum melongena L.) seedlings by regulating the glutathione-ascorbate-dependent detoxification path-way. J. Hort. Sci. Biotech. 91 (4) : 412-420.
https://doi.org/10.1080/14620316.2016.1162030
 
203. Xie G., Sasaki K., Imai R., Xie D. 2014. A redox-sensitive cysteine residue regulates the kinase activities of OsMPK3 and OsMPK6 in vitro. Plant Sci. 227 : 69-75.
https://doi.org/10.1016/j.plantsci.2014.07.002
 
204. Yadav V., Arif N., Singh S., Sri-vastava P. K., Sharma S., Tripathi D. K. 2016. Exogenous mineral regulation under heavy metal stress: advances and prospects. Bio-chem. Pharmacol. 5 (220) : 2167-0501.
https://doi.org/10.4172/2167-0501.1000220
 
205. Ye Y., Li Z., Xing D. 2013. Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Ara-bidopsis thaliana programmed cell death. Plant Cell Environ. 36 :1-15.
https://doi.org/10.1111/j.1365-3040.2012.02543.x
 
206. Ye Y., Ding, Y., Jiang Q., Wang F., Sun J., Zhu C. 2017. The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants. Plant Cell Rep. 36 : 235-242.
https://doi.org/10.1007/s00299-016-2084-x
 
207. Yu L.J., Luo Y.F., Liao B., Xie L.J., Chen L. 2012. Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to ar-senic stress in rice (Oryza sativa). New Phy-tol. 195 : 97-112.
https://doi.org/10.1111/j.1469-8137.2012.04154.x
 
208. Yuan H., Zhang Y., Huang S., Yang Y., Gu C. 2015. Effects of exogenous glutathione and cysteine on growth,lead accumulation, and tolerance of Iris lactea var. chinensis. Environ. Sci. Pollut. Res. 22 : 2808-2816.
https://doi.org/10.1007/s11356-014-3535-y
 
209. Yuan H. M., Huang X. 2016. Inhibi-tion of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Ara-bidopsis. Plant Cell Environ. 39 : 120-135.
https://doi.org/10.1111/pce.12597
 
210. Yusuf M., Fariduddin Q., Ahmad A. 2012. 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmo-lyte in tolerant and sensitive varieties of Vigna radiate under different levels of nick-el: A shotgun approach. Plant Physiol. Bio-chem. 57 : 143-153.
https://doi.org/10.1016/j.plaphy.2012.05.004
 
211. Zelinová V., Alemayehu A., Bocová B., Huttová J., Tamás L. 2015. Cadmium-induced reactive oxygen species generation, changes in morphogenic responses and ac-tivity of some enzymes in barley root tip are regulated by auxin. Biologia 70 : 356-364.
https://doi.org/10.1515/biolog-2015-0035
 
212. Zeng F., Qiu B., Wu X., Niu S., Wu F., Zhang G. 2012. Glutathione-mediated al-leviation of chromium toxicity in rice plants. Biol. Trace Elem. Res. 148 : 255-263.
https://doi.org/10.1007/s12011-012-9362-4
 
213. Zeng X., Xu X., Boezen H.M., Huo X. 2016. Children with health impairments by heavy metals in an e-waste recycling ar-ea. Chemosphere. 148 : 408-415.
https://doi.org/10.1016/j.chemosphere.2015.10.078
 
214. Zhang P.Y., Zhang Z.H., Wang J., Cong B.L., Chen K.S., Liu S.H. 2014. A novel receptor-like kinase (PnRLK-1) from the Antarctic Moss Pohlia nutans enhances salt and oxidative stress tolerance. Plant Mol. Biol. Rep. 33 : 1156-1170.
https://doi.org/10.1007/s11105-014-0823-0
 
215. Zhao F.Y., Han M.M., Zhang S.Y., Wang K., Zhang C.R., Liu T., Liu W. 2012. Hydrogen peroxide-mediated growth of the root system occurs via auxin signaling modification and variations in the expres-sion of cell-cycle genes in rice seedlings ex-posed to cadmium stress. J. Integr. Plant Bi-ol. 54 : 911-1006.
https://doi.org/10.1111/j.1744-7909.2012.01170.x
 
216. Zhao F.Y., Hu F., Zhang S.Y. 2013. MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Envi-ron. Sci. Pollut. Res. 20 : 5449-5460.
https://doi.org/10.1007/s11356-013-1559-3
 
217. Zhou J., Xia X.J., Zhou Y.H., Shi K., Chen Z., Yu J.Q. 2014. RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in accli-mation- induced cross-tolerance in tomato. J. Exp. Bot. 65 : 595-607.
https://doi.org/10.1093/jxb/ert404
 
218. Zhu X.F., Wang Z.W., Dong F., Lei G.J., Shi Y.Z., Li G.X., Zheng S.J. 2013. Ex-ogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating syn-thesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater. 263 : 98-403.
https://doi.org/10.1016/j.jhazmat.2013.09.018