Abstract
Heavy metal toxicity is one of the major agricultural concerns that can adversely affect crop growth and yield. Being sessile, plants must evolve a wide array of physio-chemical defense mechanisms to accumulate and tolerate excessive concentrations of heavy metals. These mechanisms, in turn, help in maintaining ionic balance in plant cells, which is physiologically essential for cellular functioning and metabolism. In this chapter, we comprehensively discuss these molecular mechanisms, the signaling responses involved and coordinated cross talk of different processes taking place during heavy metal uptake, translocation, sequestration, and detoxification in plants. Among the key players, recent work has revealed the vital roles played by miRNAs in supplementing metal detoxification by means of transcription factors (TF) or gene regulation. We believe that a complete understanding of the underlying mechanisms may help scientists to adopt novel molecular and genetic approaches that may pave the way for developing transgenic crops with improved heavy metal stress tolerance.
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References
Arbaoui S, Slimane RB, Rezgui S, Bettaieb T (2014) Metal transporters for uptake, sequestration and translocation. In: Gupta DK, Chatterjee S (eds) Heavy metal remediation: transport and accumulation in plants. Nova Science Publishers, New York, pp 29–44
Barbosa JTP, Santos CM, Peralva VN, Flores EM, Korn M, Nóbrega JA, Korn MGA (2015) Microwave-assisted diluted acid digestion for trace elements analysis of edible soybean products. Food Chem 175:212–217
Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MSA (2014) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res 21:717–731
Bouazizi H, Jouili H, Geitmann A, El Ferjani E (2010) Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol Environ Saf 73:1304–1308
Brunetti P, Zanella L, De Paolis A, Di Litta D, Cecchetti V, Falasca G, Barbieri M, Altamura MM, Costantino P, Cardarelli M (2015) Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J Exp Bot 66:3815–3829
Casacuberta JM, Devos Y, Du Jardin P, Ramon M, Vaucheret H, Nogue F (2015) Biotechnological uses of RNAi in plants: risk assessment considerations. Trends Biotechnol 33:145–147
Chen L, Wang T, Zhao M, Tian Q, Zhang WH (2012) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235:375–386
Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356
Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245
Chmielowska-Bąk J, Arasimowicz-Jelonek M, Izbiańska K, Frontasyeva M, Zinicovscaia I, Guiance-Varela C, Deckert J (2017) NADPH oxidase is involved in regulation of gene expression and ROS overproduction in soybean (Glycine max L.) seedlings exposed to cadmium. Acta Soc Bot Pol 86(2):3551
Choppala G, Saifullah BN, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391
Cohen MD, Prophete C, Sisco M, Chen LC, Zelikoff JT, Smee JJ, Holder AA, Crans DC (2006) Pulmonary immunotoxic potentials of metals are governed by select physicochemical properties: chromium agents. J Immunotoxicol 3:69–81
Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2008) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. AoB Plants 103:1–11
Çelik Ö, Akdaş EY (2019) Tissue-specific transcriptional regulation of seven heavy metal stress-responsive miRNAs and their putative targets in nickel indicator castor bean (R. communis L.) plants. Ecotoxicol Environ Saf 170:682–690
DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132
Diatloff E, Forde BG, Roberts SK (2006) Expression and transport characterisation of the wheat low-affinity cation transporter (LCT1) in the methylotrophic yeast Pichia pastoris. Biochem Biophys Res Commun 344:807–813
Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573
Ding Y, Gong S, Wang Y, Wang F, Bao H, Sun J, Cai C, Yi K, Chen Z, Zhu C (2018) MicroRNA166 modulates cadmium tolerance and accumulation in rice. Plant Physiol 177(4):1691–1703
Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120
Fan SK, Fang XZ, Guan MY, Ye YQ, Lin XY, Du ST, Jin CW (2014) Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5:721
Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472
Gautam M, Pandey D, Agrawal SB, Agrawal M (2016) Metals from mining and metallurgical industries and their toxicological impacts on plants. In: Singh A, Prasad SM, Singh RP (eds) Plant responses to xenobiotics. Springer, Singapore, pp 231–272
Greger M (2004) Metal availability, uptake, transport and accumulation in plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Springer, New York, pp 1–27
Gu CS, Liu LQ, Deng YM, Zhu XD, Huang SZ, Lu XQ (2015) The heterologous expression of the Iris lactea var. chinensis type 2 metallothionein IlMT2b gene enhances copper tolerance in Arabidopsis thaliana. Bull Environ Contam Toxicol 94:247–253
Gupta DK, Vandenhove H, Inouhe M (2013) Role of phytochelatins in heavy metal stress and detoxification mechanisms in plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg, pp 73–94
He JY, Ren YF, Cheng ZHU, Jiang DA (2008) Effects of cadmium stress on seed germination, seedling growth and seed amylase activities in rice (Oryza sativa). Rice Sci 15:319–325
Hossain Z, Komatsu S (2013) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310
Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43:2393–2416
Huang SQ, Xiang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8:887–899
Huang TL, Nguyen QTT, Fu SF, Lin CY, Chen YC, Huang HJ (2012) Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80:587–608
Huang Y, Chen Q, Deng M, Japenga J, Li T, Yang X, He Z (2018a) Heavy metal pollution and health risk assessment of agricultural soils in a typical peri-urban area in southeast China. J Environ Manag 207:159–168
Huang Y, Fang Y, Long X, Liu L, Wang J, Zhu J, Ma Y, Qin Y, Qi J, Hu X, Tang C (2018b) Characterization of the rubber tree metallothionein family reveals a role in mitigating the effects of reactive oxygen species associated with physiological stress. Tree Physiol. 38: 911–924
Islam E, Khan MT, Irem S (2015) Biochemical mechanisms of signaling: perspectives in plants under arsenic stress. Ecotoxicol Environ Saf 114:126–133
Jagadeeswaran G, Li YF, Sunkar R (2014) Redox signaling mediates the expression of a sulfate-deprivation-inducible microRNA395 in Arabidopsis. Plant J 77:85–96
Jain S, Muneer S, Guerriero G, Liu S, Vishwakarma K, Chauhan DK, Dubey NK, Tripathi DK, Sharma S (2019) Tracing the role of plant proteins in the response to metal toxicity: a comprehensive review. Plant Signal Behav 13(9):e1507401
Joshi R, Pareek A, Singla-Pareek SL (2015) Plant Metallothioneins: Classification, Distribution, Function, and Regulation. In: Ahmad P (ed), Plant Metal Interaction, Elsevier, Amsterdam, Netherlands, pp 239–261
Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029
Joshi R, Gupta P, Singla-Pareek SL, Pareek A (2017) Biomass production and salinity response in plants: role of MicroRNAs. Indian J Plant Physiol 22:448–457
Khan DA, Ali Z, Iftikhar S, Amraiz D, Gul A, Babar MM (2018) Role of phytohormones in enhancing antioxidant defense in plants exposed to metal/metalloid toxicity. In: Hasanuzzaman M, Nahar K, Fujita M (eds) Plants under metal and metalloid stress. Springer, Singapore, pp 367–400
Kısa D, Elmastaş M, Öztürk L, Kayır Ö (2016a) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59:813–820
Kısa D, Öztürk L, Tekin Ş (2016b) Gene expression analysis of metallothionein and mineral elements uptake in tomato (Solanum lycopersicum) exposed to cadmium. J Plant Res 129:989–995
Kohli SK, Handa N, Gautam V, Bali S, Sharma A, Khanna K, Arora S, Thukral AK, Ohri P, Karpets YV, Kolupaev YE (2017) ROS signaling in plants under heavy metal stress. In: Khan MIR, Khan NA (eds) Reactive oxygen species and antioxidant systems in plants: role and regulation under abiotic stress. Springer, Singapore, pp 185–214
Kovács V, Gondor OK, Szalai G, Darkó É, Majláth I, Janda T, Pál M (2014) Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. J Hazard Mater 280:12–19
Kozhevnikova AD, Seregin IV, Erlikh NT, Shevyreva TA, Andreev IM, Verweij R, Schat H (2014) Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 203:508–519
Kumar A, Aery NC (2016) Impact, metabolism, and toxicity of heavy metals in plants. In: Plant responses to xenobiotics. Springer, Singapore, pp 141–176
Kumar G, Kushwaha HR, Panjabi-Sabharwal V, Kumari S, Joshi R, Karan R, Mittal S, Pareek SLS, Pareek A (2012) Clustered metallothionein genes are co-regulated in rice and ectopic expression of OsMT1e-P confers multiple abiotic stress tolerance in tobacco via ROS scavenging. BMC Plant Biol 12:107
Kumar D, Singh DP, Barman SC, Kumar N (2016) Heavy metal and their regulation in plant system: an overview. In: Singh A, Prasad SM, Singh RP (eds) Plant responses to xenobiotics. Springer, Singapore, pp 19–38
Kushwaha A, Rani R, Kumar S, Gautam A (2015) Heavy metal detoxification and tolerance mechanisms in plants: implications for phytoremediation. Environ Rev 24:39–51
Lai X, Stigliani A, Vachon G, Carles C, Smaczniak C, Zubieta C, Kaufmann K, Parcy F (2018) Building transcription factor binding site models to understand gene regulation in plants. Mol Plant. https://doi.org/10.1016/j.molp.2018.10.010
Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800
Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694
Li T, Li H, Zhang YX, Liu JY (2010) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833
Lima J, Arenhart RA, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817–2832
Liu J, Shi X, Qian M, Zheng L, Lian C, Xia Y, Shen Z (2015) Copper-induced hydrogen peroxide upregulation of a metallothionein gene, OsMT2c, from Oryza sativa L. confers copper tolerance in Arabidopsis thaliana. J Hazard Mater 294:99–108
Liu Z, Ding Y, Wang F, Ye Y, Zhu C (2016) Role of salicylic acid in resistance to cadmium stress in plants. Plant Cell Rep 35(4):719–731
Lomaglio T, Rocco M, Trupiano D, De Zio E, Grosso A, Marra M, Delfine S, Chiatante D, Morabito D, Scippa GS (2015) Effect of short-term cadmium stress on Populus nigra L. detached leaves. J Plant Physiol 182:40–48
Luo ZB, Wu C, Zhang C, Li H, Lipka U, Polle A (2014) The role of ectomycorrhizas in heavy metal stress tolerance of host plants. Environ Exp Bot 108:47–62
Luo ZB, He J, Polle A, Rennenberg H (2016) Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv 34:1131–1148
Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals. Springer briefs in molecular science. Springer, Dordrecht, pp 27–53
Mekawy AMM, Assaha DV, Munehiro R, Kohnishi E, Nagaoka T, Ueda A, Saneoka H (2018) Characterization of type 3 metallothionein-like gene (OsMT-3a) from rice, revealed its ability to confer tolerance to salinity and heavy metal stresses. Environ Exp Bot 147:157–166
Michel-Lopez C, Zapata-Pérez O, González-Mendoza D, Grimaldo-Juarez O, Ceceña-Duran C, Tzintzun-Camacho O (2017) Expression of metallothionein type 2 and 3 genes in Prosopis glandulosa leaves treated with copper. Genet Mol Res 16:gmr16019490
Migeon A, Blaudez D, Wilkins O, Montanini B, Campbell MM, Richaud P, Thomine S, Chalot M (2010) Genome-wide analysis of plant metal transporters, with an emphasis on poplar. Cell Mol Life Sci 67:3763–3784
Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381
Monferrán MV, Wunderlin DA (2013) Biochemistry of metals/metalloids toward remediation process. In: Gupta D, Corpas F, Palma J (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg, pp 43–71
Mustafa G, Komatsu S (2016) Toxicity of heavy metals and metal-containing nanoparticles on plants. BBA – Proteins and Proteomics 1864:932–944
Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442
Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24:10068–10082
Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2012) Mitogen-activated protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int J Mol Sci 13:7828–7853
Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32:73–86
Palma JM, Gupta DK, Corpas FJ (2013) Metalloenzymes involved in the metabolism of reactive oxygen species and heavy metal stress. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg, pp 1–17
Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants. Front Plant Sci 6:232
Pérez-Chaca MV, Rodríguez-Serrano M, Molina AS, Pedranzani HE, Zirulnik F, Sandalio LM, Romero-Puertas MC (2014) Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant Cell Environ 37:1672–1687
Pilon M (2017) The copper microRNAs. New Phytol 213:1030–1035
Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg, pp 121–147
Prakash V, Saxena S (2017) Molecular overview of heavy metal phytoremediation. In: Bhakta JK (ed) Handbook of research on inventive bioremediation techniques. IGI Global, India, pp 247–263
Rai R, Agrawal M, Agrawal SB (2016) Impact of heavy metals on physiological processes of plants: with special reference to photosynthetic system. In: Singh A, Prasad SM, Singh RP (eds) Plant responses to xenobiotics. Springer, Singapore, pp 127–140
Rout GR, Panigrahi J (2015) Analysis of signaling pathways during heavy metal toxicity: a functional genomics perspective. In: Pandey GK (ed) Elucidation of abiotic stress signaling in plants. Springer, New York, pp 295–322
Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38
Saraswat S, Rai JPN (2011) Complexation and detoxification of Zn and Cd in metal accumulating plants. Rev Environ Sci Bio-Technol 10:327–339
Saxena P, Misra N (2010) Remediation of heavy metal contaminated tropical land. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Berlin, Heidelberg, pp 431–477
Seneviratne M, Weerasundara L, Ok YS, Rinklebe J, Vithanage M (2017) Phytotoxicity attenuation in Vigna radiata under heavy metal stress at the presence of biochar and N fixing bacteria. J Environ Manag 186:293–300
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50
Sharma SS, Dietz KJ, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39(5):1112–1126
Shaw BP, Sahu SK, Mishra RK (2004) Heavy metal induced oxidative damage in terrestrial plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg, pp 84–126
Shi WG, Li H, Liu TX, Polle A, Peng CH, Luo ZB (2015) Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant Cell Environ 38:207–223
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143
Song Y, Cui J, Zhang H, Wang G, Zhao FJ, Shen Z (2013) Proteomic analysis of copper stress responses in the roots of two rice (Oryza sativa L.) varieties differing in Cu tolerance. Plant Soil 366:647–658
Srivastava S, Suprasanna P, D’souza SF (2012) Mechanisms of arsenic tolerance and detoxification in plants and their application in transgenic technology: a critical appraisal. Int J Phytoremediation 14:506–517
Tamás L, Mistrík I, Alemayehu A, Zelinová V, Bočová B, Huttová J (2015) Salicylic acid alleviates cadmium-induced stress responses through the inhibition of Cd-induced auxin-mediated reactive oxygen species production in barley root tips. J Plant Physiol 173:1–8
Thakur S, Singh L, Ab-Wahid Z, Siddiqui MF, Atnaw SM, Din MFM (2016) Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess 188:206
Thornalley PJ, Vašák M (1985) Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. BBA-Protein Struct Molecular Enzymol 827:36–44
Tripathi P, Singh PK, Mishra S, Gautam N, Dwivedi S, Chakrabarty D, Tripathi RD (2015) Recent advances in the expression and regulation of plant metallothioneins for metal homeostasis and tolerance. In: Chandra R (ed) Environmental waste management. CRC Press, Boca Raton, pp 551–564
Tsednee M, Yang SC, Lee DC, Yeh KC (2014) Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiol 166:839–852
Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233
Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10(3):268–292
Wagatsuma T (2017) The membrane lipid bilayer as a regulated barrier to cope with detrimental ionic conditions: making new tolerant plant lines with altered membrane lipid bilayer. Soil Sci Plant Nutr 63(5):507–516
Wang R, Wang J, Zhao L, Yang S, Song Y (2015) Impact of heavy metal stresses on the growth and auxin homeostasis of Arabidopsis seedlings. Biometals 28:123–132
Wang J, Fang Y, Tian B, Zhang X, Zeng D, Guo L, Hu J, Xue D (2018) New QTLs identified for leaf correlative traits in rice seedlings under cadmium stress. Plant Growth Regul 85(2):329–335
Weerakoon SR (2019) Genetic engineering for metal and metalloid detoxification. In: Prasad MNV (ed) Transgenic plant technology for remediation of toxic metals and metalloids. Academic Press, London, pp 23–41
Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5:60
Wianowska D, Maksymiec W, Dawidowicz AL, Tukiendorf A (2004) The influence of heavy metal stress on the level of some flavonols in the primary leaves of Phaseolus coccineus. Acta Physiol Plant 26:247–254
Wu L, Yu J, Shen Q, Huang L, Wu D, Zhang G (2018) Identification of microRNAs in response to aluminum stress in the roots of Tibetan wild barley and cultivated barley. BMC Genomics 19(1):560
Xu J, Yin H, Li Y, Liu X (2010) Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol 154:1319–1334
Xu J, Sun J, Du L, Liu X (2012) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124
Yamaguchi N, Mori S, Baba K, Kaburagi-Yada S, Arao T, Kitajima N, Hokura A, Terada Y (2011) Cadmium distribution in the root tissues of solanaceous plants with contrasting root-to-shoot Cd translocation efficiencies. Environ Exp Bot 71:198–206
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein–like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361
Yu LJ, Luo YF, Liao B, Xie LJ, Chen L, Xiao S, Li JT, Hu SN, Shu WS (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol 195:97–112
Zaheer IE, Ali S, Rizwan M, Farid M, Shakoor MB, Gill RA, Najeeb U, Iqbal N, Ahmad R (2015) Citric acid assisted phytoremediation of copper by Brassica napus L. Ecotoxicol Environ Saf 120:310–317
Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159:84–91
Zeng QY, Yang CY, Ma QB, Li XP, Dong WW, Nian H (2012) Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol 12:182
Zhang XD, Sun JY, You YY, Song JB, Yang ZM (2018) Identification of Cd-responsive RNA helicase genes and expression of a putative BnRH 24 mediated by miR158 in canola (Brassica napus). Ecotoxicol Environ Saf 157:159–168
Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, Zhong W, Wu P (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686
Zhou ZS, Song JB, Yang ZM (2012a) Genome wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 63:4597–4613
Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P, Lu S, Li F, Zhu L, Liu Z, Chen L (2012b) Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22:649
Acknowledgments
RJ would like to acknowledge Dr D S Kothari Postdoctoral Fellowship from UGC. AP and SLS-P are supported by funding from the Indo-US Science and Technology Forum (IUSSTF) for Indo-US Advanced Bioenergy Consortium (IUABC). Research in the lab of AP is also supported from funds received from International Atomic Energy Agency (Vienna), UGC-RNW, and UPE-II, JNU.
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Joshi, R., Dkhar, J., Singla-Pareek, S.L., Pareek, A. (2019). Molecular Mechanism and Signaling Response of Heavy Metal Stress Tolerance in Plants. In: Srivastava, S., Srivastava, A., Suprasanna, P. (eds) Plant-Metal Interactions. Springer, Cham. https://doi.org/10.1007/978-3-030-20732-8_2
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