Abstract
Among abiotic stress, the toxicity of metals impacts negatively on plants’ growth and productivity. This toxicity promotes various perturbations in plants at different levels. To withstand stress, plants involve efficient mechanisms through the implication of various signaling pathways. These pathways enhance the expression of many target genes among them gene coding for metal transporters. Various metal transporters which are localized at the plasma membrane and/or at the tonoplast are crucial in metal stress response. Furthermore, metal detoxification is provided by metal-binding proteins like phytochelatins and metallothioneins. The understanding of the molecular basis of metal toxicities signaling pathways and tolerance mechanisms is crucial for genetic engineering to produce transgenic plants that enhance phytoremediation. This review presents an overview of the recent advances in our understanding of metal stress response. Firstly, we described the effect of metal stress on plants. Then, we highlight the mechanisms involved in metal detoxification and the importance of the regulation in the response to heavy metal stress. Finally, we mentioned the importance of genetic engineering for enhancing the phytoremediation technique. In the end, the response to heavy metal stress is complex and implicates various components. Thus, further studies are needed to better understand the mechanisms involved in response to this abiotic stress.
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The data supporting this review are from previously reported studies, which have been cited in this manuscript.
Abbreviations
- ABA:
-
Abscisic acid
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- ACO:
-
ACC oxidase
- ACS:
-
ACC synthases
- AMF:
-
Arbuscular mycorrhizal fungi
- CaMs:
-
Calmodulins
- CBLs:
-
Calcineurin B-like proteins
- CDF:
-
Cation diffusion facilitator transporter
- CDPKs:
-
Ca2+-dependent protein kinases
- CIPK:
-
CBL-interacting proteins kinases
- CTR1:
-
Constitutive triple response 1
- DRE:
-
Dehydration-responsive elements
- DREB:
-
Drought-responsive elements binding
- ERF:
-
Ethylene-responsive factors
- ET:
-
Ethylene
- ETR1:
-
Ethylene resistant 1
- GST:
-
Glutathione S-transferase
- HSPs:
-
Heat shock proteins
- HMAs:
-
Heavy metal transport ATPases
- JA:
-
Jasmonate
- MAPK:
-
Mitogen-activated protein kinase
- MTP:
-
Metal tolerance protein
- MTs:
-
Metallothioneins
- Nramp:
-
Natural resistance-associated macrophage protein
- PCs:
-
Phytochelatins
- PGPR:
-
Beneficial plant growth-promoting bacteria
- QTL:
-
Quantitative trait loci
- ROS:
-
Reactive oxygen species
- SAM:
-
S-Adenosyl-methionine
References
Abdelkrim S, Jebara SH, Saadani O et al (2020) In situ effects of Lathyrus sativus- PGPR to remediate and restore quality and fertility of Pb and Cd polluted soils. Ecotoxicol Environ Saf 192:110260
Adamowski M, Friml J (2015) PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32
Ahsan N, Renaut J, Komatsu S (2009) Recent developments in the application of proteomics to the analysis of plant responses to heavy metal. Proteomics 9:2602–2621
Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 121:472–480
Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chemi 2019:14
Ali S, Abbas Z, Seleiman MF et al (2020) Glycine betaine accumulation, significance and interests for heavy metal tolerance in plants. Plants 9:896
Alotaibi MO, Mohammed AE, Almutairi T, Elobeid MM (2019) Morpho-physiological and proteomic analyses of Eucalyptus camaldulensis as a bioremediator in copper-polluted soil in Saudi Arabia. Plants 8:43
Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182
Arif N, Yadav V, Singh S, Singh S, Ahmad P, Mishra RK, Sharma S, Tripathi DK, Dubey NK, Chauhan DK (2016) Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Front Environ Sci 4:69
Arif N, Sharma NC, Yadav V et al (2019) Understanding heavy metal stress in a rice crop: toxicity, tolerance mechanisms, and amelioration strategies. J Plant Biol 62:239–253
Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20:1390–1406
Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61
Aung MS, Masuda H, Nozoye T, Kobayashi T, Jeon JS, An G, Nishizawa NK (2019) Nicotianamine synthesis by OsNAS3 is important for mitigating iron excess stress in rice. Front Plant Sci 10:660
Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps inArabidopsis. Plant Physiol 126:696–706
Azzarello E, Pandolfi C, Giordano C et al (2012) Ultramorphological and physiological modifications induced by high zinc levels in Paulownia tomentosa. Environ Exp Bot 81:11–173
Baliardini C, Meyer CL, 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
Ban Q, Liu G, Wang Y (2011) A DREB gene from Limonium bicolor mediates molecular and physiological responses to copper stress in transgenic tobacco. J Plant Physiol 168:449–458
Benatti RM, Yookongkaew N, Meetam M et al (2014) Metallothionein deficiency impacts copper accumulation and redistribution in leaves and seeds of Arabidopsis. New Phyto 202:940–951
Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148
Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci U S A 106:8067–8072
Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Lee Y, Liu JR (2011) Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation. Plant Cell Tissue Organ Cult 107:69–77
Briffa J, Sinagra E, Blundell R (2020) heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6:e04691
Brunetti P, Zanella L, De Paolis A et al (2015) Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J Exp Bot 66:3815–3829
Cailliatte R, Lapeyre B, Briat J-F, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228
Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17
Cao S, Chen Z, Liu G, Jiang L, Yuan H, Ren G, Bian X, Jian H, Ma X (2009) The Arabidopsis ethylene-insensitive 2 gene is required for lead resistance. Plant Physiol Biochem 47:308–312
Cao F, Dai H, Hao PF, Wu F (2020) Silicon regulates the expression of vacuolar H+-pyrophosphatase 1 and decreases cadmium accumulation in rice (Oryza sativa L.). Chemosphere 240:124907
Capdevila M, Atrian S (2011) Metallothionein protein evolution: a mini-assay. J Biol Inorg Chem 16:977–989
Carini F, Bengtsson G (2001) Postdeposition transport of radionuclides in fruit. J Environ Radioact 52:215–236
Ceasar SA, Lekeux G, Motte P et al (2020) di-Cysteine residues of the Arabidopsis thaliana HMA4 C-terminus are only partially required for cadmium transport. Front Plant Sci 11:560
Charfeddine M, Charfeddine S, Bouaziz D, Messaoud RB, Bouzid RG (2017) The effect of cadmium on transgenic potato (Solanum tuberosum) plants overexpressing the StDREB transcription factors. Plant Cell Tissue Organ Cult 128:521–541
Chaturvedi AK, Patel MK, Mishra A, Tiwari V, Jha B (2014) The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco. PLoS ONE 9(10):e111379
Chen YA, Chi WC, Huang TL, Lin CY et al (2012) Mercury-induced biochemical and proteomic changes in rice roots. Plant Physiol Biochem 55:23–32
Chen YA, Chi WC, Trinh NN, Huang LY, Chen YC, Cheng KT et al (2014) Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings. PLoS ONE 9:e95163
Chen C, Song Y, Zhuang K, Li L, Xia Y, Shen Z (2015) Proteomic analysis of copper-binding proteins in excess copper-stressed roots of two rice (Oryza sativa L.) varieties with different Cu tolerances. PLoS ONE 10(4):e0125367
Cho D, Villiers F, Kroniewicz L et al (2012) Vacuolar CAX1 and CAX3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol 160:1293–1302
Clemens S (2006) Evolution and function of phytochelatin synthases. J Plant Physiol 163:319–332
Cong W, Miao Y, Xu L et al (2019) Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol 19:282
Conn SJ, Gilliham M, Athman A et al (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23:240–257
D’Alessandro A, Taamalli M, Gevi F, Timperio AM, Zolla L, Ghnaya T (2013) Cadmium stress responses in Brassica juncea: hints from proteomics and metabolomics. J Proteom Res 12:4979–4997
Dai J, Wang N, Xiong H, Qiu W, Nakanishi H, Kobayashi T, Nishizawa NK, Zuo Y (2018) The yellow stripe-like (YSL) gene functions in internal copper transport in peanut. Genes 9:635
DalCorso G, Fasasni E, Furini A (2013) Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics. Fron Plant Sci 4:280
Das N, Bhattacharya S, Maiti MK (2016) Enhanced cadmium accumulation and tolerance in transgenic tobacco overexpressing rice metal tolerance protein gene OsMTP1 is promising for phytoremediation. Plant Physiol Biochem 105:297–309
Delhaize E, Kataoka T, Hebb DM, White RG, Ryan PR (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15:1131–1142
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 H, Gao J, Qin C, Ma H et al (2014) The dynamics of DNA methylation in maize roots under Pb stress. Int J Mol Sci 15:23537–23554
Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma virensenhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6(1):e16360
Djemal R, Khoudi H (2021) The ethylene-responsive transcription factor of durum wheat, TdSHN1, confers cadmium, copper, and zinc tolerance to yeast and transgenic tobacco plants. Protoplasma. https://doi.org/10.1007/s00709-021-01635-z
Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper induced oxidative stress and antioxidant defense in Arabidopsis thaliana. Biometals 17:379–387
Elbaz B, Shoshani-Knaani N, David-Assael O et al (2006) High expression in leaves of the zinc hyperaccumulator Arabidopsis helleri of AhMHX, a homolog of an Arabidopsis thaliana vacuolar metal/proton exchanger. Plant Cell Environ 29:1179–1190
Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P(1B)- type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723
Faè M, Balestrazzi A, Confalonieri M, Donà M, Macovei A, Valassi A, Carbonera D (2014) Copper-mediated genotoxic stress is attenuated by the overexpression of the DNA repair gene MtTdp2α (tyrosyl-DNA phosphodiesterase 2) in Medicago truncatula plants. Plant Cell Rep 33:1071–1080
Fan W, Liu C, Cao B et al (2018) Genome-wide identification and characterization of four gene families putatively involved in cadmium uptake, translocation and sequestration in Mulberry. Front Plant Sci 9:879
Farinati S, DalCorso G, Varotto S, Furini A (2010) The brassica juncea BjCdR15, an ortholog of Arabidopsis TGA3, is a regulator of cadmium uptake, transport and accumulation in shoots and confers cadmium tolerance in transgenic plants. New Phytol 185:964–978
Feki K, Kamoun Y, Ben Mahmoud R, Farhat-Khemakhem A, Gargouri A, Brini F (2015) Multiple abiotic stress tolerance of the transformants yeast cells and the transgenic Arabidopsis plants expressing a novel durum wheat catalase. Plant Physiol Bioch 97:420–431
Feng RW, Wang L, Yang JG, Zhao PP et al (2021) Underlying mechanisms responsible for restriction of uptake and translocation of heavy metals (metalloids) by selenium via root application in plants. J Hazard Mater 402:123570
Fernández V, Brown PH (2013) From plant surface to plant metabolism: the uncertain fate of foliar applied nutrients. Front Plant Sci 4:289
Fu S, Lu Y, Zhang X et al (2019) The ABC transporter ABCG36 is required for cadmium tolerance in rice. J Exp Bot 70:5909–5918
Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 56:3017–3027
Gaillard S, Jacquet H, Vavasseur A, Leonhardt N, Forestier C (2008) AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol 8:22
Gaitán-Solís E, Taylor NJ, Siritunga D, Stevens W, Schachtman DP (2015) Overexpression of the transporters AtZIP1 and AtMTP1 in cassava changes zinc accumulation and partitioning. Front Plant Sci 6:492
Gao X, Ai WL, Gong H, Cui LJ, Chen BX, Luo HY, Qiu BS (2016) Transgenic NfFeSOD Sedum alfredii plants exhibited profound growth impairments and better relative tolerance to long-term abiotic stresses. Plant Biotechnol Rep 10:117–128
Gao Y, Yang F, Liu J, Xie W, Zhang L, Chen Z, Peng Z, Ou Y, Yao Y (2020) Genome-wide identification of metal tolerance protein genes in Populus trichocarpa and their roles in response to various heavy metal stresses. Int J Mol Sci 21:1680
Gendre D, Czernic P, Conejero G, Pianelli K, Briat J, Lebrun M (2006) TcYSL3, a member of the YSL Gene Family from the Hyperaccumulator Thlaspi caerulescens, encodes a nicotianamine Ni/Fe transporter. Plant J49:1–15
Głowacka K, Sokolnik AZ, Okorski A, Najdzion J (2019) The effect of cadmium on the activity of stress-related enzymes and the ultrastructure of pea roots. Plants 8:413
Goix S, Lévêque T, Xiong TT, Schreck E, Baeza-Squiban A, Geret F, Uzu G, Austruy A, Dumat C (2014) Environmental and health impacts of fine and ultrafine metallic particles: assessment of threat scores. Environ Res 133:185–194
Gong X, Liu Y, Huang D, Zeng G, Liu S, Tang H et al (2016) Effects of exogenous calcium and spermidine on cadmium stress moderation and metal accumulation in Boehmeria nivea (L.) Gaudich. Environ Sci Pollut Res 23:8699–8708
Goto F, Enomoto Y, Shoji K, Shimada H, Yoshihara T (2019) Copper treatment of peach leaves causes lesion formation similar to the biotic stress response. Plant Biotechnol 36:135–142
Gouiaa S, Khoudi H (2019) Expression of V-PPase proton pump, singly or in combination with a NHX1 transporter, in transgenic tobacco improves copper tolerance and accumulation. Environ Sci Pollut Res 26:37037–37045
Grauwe DL, Dugardeyn J, Straeten DVD (2008) Novel mechanisms of ethylene-gibberellin crosstalk revealed by the gai eto2-1 double mutant. Plant Signal Behav 3:1113–1115
Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561:22–28
Guan Z, Chai T, Zhang Y, Xu J, Wei W (2009) Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76(5):623–630
Guerrero MG, Escudero V, Saez A, Jimenez MT (2016) Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia. Front Plant Sci 7:1088
Guo J, Xu W, Ma M (2012) The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J Hazard Mater 15:309–313
Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384
Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J et al (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198
Hanaka A, Wojcik M, Dresler S, Mroczek-Zdyrska M, Maksymiec W (2016) Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with Cu? Ecotoxicol Environ Saf 124:480–488
Hasan MK, Cheng Y, Kanwar MK, Chu XY, Ahammed GJ, Qi ZY (2017) Responses of plant proteins to heavy metal Stress-A Review. Front Plant Sci 8:1492
Hattab S, Dridi B, Chouba L, Kheder MB, Bousetta H (2009) Photosynthesis and growth responses of pea Pisum sativum L. under heavy metals stress. J Environ Sci 21:1552–1556
He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108:114–119
Hermans C, Conn SJ, Chen J, Xiao Q, Verbruggen N (2013) An update on magnesium homeostasis mechanismsin plants. Metallomics 5:1170–1183
Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, Mori S (2001) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J 25:159–167
Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133
Hossain Z, Komatsu S (2013) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310
Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:872875
Huang TL, Huang HJ (2008) ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere 71:1377–1385
Hussain D, Haydon MJ, Wang Y et al (2004) P-Type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Impa SM, Johnson-Beebout SE (2012) Mitigating zinc deficiency and achieving high grain Zn in rice through integration of soil chemistry and plant physiology research. Plant Soil 361:3–41
Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2003) Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J 36:366–381
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T et al (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286
Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816
Jalmi SK, Bhagat PK, Verma D et al (2018) Traversing the link between heavy metal stress and plant signaling. Front Plant Sci 9:12
Jin Sh, Xu Ch, Li G et al (2017) Functional characterization of a type 2 metallothionein gene, SsMT2, from alkaline-tolerant Suaeda salsa. Sci Rep 17914:1–12
Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276–3283
Kang YJ (2006) Metallothionein redox cycle and function. Exp Biol Med 231:1459–1467
Kapoor D, Kavani K, Rattan A, Landi M (2021) Ameliorative role of pre-sowing proline treatment in Coriandrum sativum l. Seedlings under mercury toxicity. Phyton 90:489–501
Kaur G, Singh HP, Batish DR, Kohli RK (2013) Lead (Pb) induced biochemical and ultrastructural changes in wheat (Triticum aestivum) roots. Protoplasma 1:53–62
Kerkeb L, Kramer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724
Keunen E, Schellingen K, Vangronsveld J, Cuypers A (2016) Ethylene and metal stress: Small molecule, big impact. Front Plant Sci 7:23
Khademi S, Khavari-Nejad RA, Saadatmand S, Najafi F (2014) The effects of exogenous salicylic acid in the antioxidant defense system in canola plants (Brassica napus L.) exposed to copper. Int J Biosci 5:64–73
Khan MS, Yu X, Kikuchi A, Asahina M, Watanabe KN (2009) Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol 26:125–134
Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530
Kim S, Takahashi M, Higuchi K, Tsunoda K, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2005) Increased Nicotianamine biosynthesis confers enhanced tolerance of high levels of metals in particular nickel to plants. Plant Cell Physiol 46:1809–1818
Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218
Kobae Y, Uemura T, Sato MH et al (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758
Kohli S, Handa N, Gautam V et al (2017) ROS signaling in plants under heavy metal stress. Reactive oxygen species and antioxidant systems in plants: role and regulation under abiotic stress, pp 185–214
Kollárová K, Kamenicka V, Vatehova Z, Lišková D (2018) Impact of galactoglucomannan oligosaccharides and Cd stress on maize root growth parameters, morphology, and structure. J Plant Physiol 222:59–66
Korenkov V, Hirschi K, Crutchfield JD, Wagner GJ (2007) Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226:1379–1387
Korenkov V, King B, Hirschi K, Wagner GJ (2009) Root-selective expression of AtCAX4 and AtCAX2 results in reduced lamina cadmium in field-grown Nicotiana tabacum L. Plant Biotechnol J 7:219–226
Kovács V, Gondor OK, Szalai G, Darkó E, 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
Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945
Kozminska A, Wiszniewska A, Fajerska EH, Muszyńska E (2018) Recent strategies of increasing metal tolerance and phytoremediation potential using genetic transformation of plants. Plant Biotech Rep 12:1–14
Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Krishna TPA, Maharajan T, Roch GV, Ignacimuthu S, Ceasar SA (2020) Structure, function, regulation and phylogenetic relationship of ZIP family transporters of plants. Front Plant Sci 11:662
Krupa Z (1999) Cadmium against higher plant photosynthesis- A variety of effects and where do they possibly come from? Z Naturforsch 54:723–729
Krzeslowska M, Lenartowska M, Mellerowicz E, Samardakiewicz S, Wozny A (2009) Pectinous cell wall thickenings formation – a response of moss protonemata cells to lead. Environ Exp Bot 65:119–131
Kumar K, Sinha AK (2013) Overexpression of constitutively active mitogen activated protein kinase kinase 6 enhances tolerance to salt stress in rice. Rice 6:25
Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751
Lanquar V, Lelièvre F, Bolte S et al (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051
Lee JH (2013) An overview of phytoremediation as a potentially promising technology for environmental pollution control. Biotechnol Bioprocess Eng 18:431–439
Lee S, Moon JS, Ko TS, Petros D, Goldsbrough PB, Korban S (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663
Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638
Lee K, Bae DW, Kim SH, Han HJ, Liu X, Park HC, Lim CO, Lee SY, Chung WS (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167:161–168
Lekeux G, Crowet JM, Nouet C et al (2019) Homology modeling and in vivo functional characterization of the zinc permeation pathway in a heavy metal P-type ATPase. J Exp Bot 70:329–341
Leszczyszyn OI, Imam HT, Blindauer CA (2013) Diversity and distribution of plant metallothioneins: a review of structure, properties and functions. Metallomics 5:1146–1169
Li G, Meng X, Wang R, Mao G, Han L, Liu Y et al (2012) Dual level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8:e1002767
Li B, Quan-Wang C, Liu H, Li HX, Yang J, Song WP, Chen L, Zeng M (2014) Effect of Cd2+ ions on root anatomical structure of four rice genotypes. J Environ Biol 35:751–757
Li P, Zhao C, Zhang Y et al (2015) Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma 253:185–200
Li X, Zhang H, Ai Q, Liang G, Yu D (2016) Two bHLH transcription factors, bHLH34 and bHLH104, regulate iron homeostasis in Arabidopsis thaliana. Plant Physiol 170:2478–2493
Li Z, Han X, Song X, Zhang Y, Jiang J, Han Q, Liu M, Qiao G, Zhuo R (2017) Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic Arabidopsis. Front Plant Sci 8:1010
Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC et al (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404
Lin T, Yang W, Lu W, Wang Y, Qi X (2017) Transcription factors PvERF15 and PvMTF-1 form a cadmium stress transcriptional pathway 1. Plant Physiol 173:1565–1573
Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399
Liu D, Xue P, Meng Q, Zou J, Gu J, Jiang W (2009) Pb/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L. Plant Cell Rep 28:695–702
Liu H, Zhao H, Wu L et al (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698
Liu XS, Feng SJ, Zhang BQ et al (2019) OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol 19:283
López-Millán AF, Ellis DR, Grusak MA (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol Biol 54:583–596
Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42
Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B–like proteins calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400
Lv YY, Deng XP, Quan LT, Xia Y, Shen ZG (2013) Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana. Plant Soil 367:507–519
Ma J, Sheng H, Li X, Wang L (2016) iTRAQ-based proteomic analysis reveals the mechanisms of silicon mediated. Plant Physiol Biochem 104:71–80
Mari S, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat JF, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111–4122
Mei H, Cheng NH, Zhao J et al (2009) Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol 183:95–105
Mendoza SAB, Sanchez F, Hernandez G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:105
Mészáros P, Rybanský L, Spieß N, Socha P, Kuna R, Libantová J, Moravčíková J, Piršelová B, Hauptvogel P, Matušíková I (2014) Plant chitinase response to different metal-type stresses reveal specificity. Plant Cell Rep 33:1789–1799
Meyer CL, Verbruggen N (2012) The use of the model species Arabidopsis halleri towards phytoextraction of cadmium polluted soils. New Biotechnol 30:9–14
Mhamdi A, Hager J, Chaouch S et al (2010) Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160
Mills RF, Francini A, Ferreira da Rocha PSC et al (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791
Mills RF, Valdes B, Duke M et al (2010) Functional significance of AtHMA4 C-terminal domain in planta. PLoS One 5(10):e13388
Mills RF, Peaston KA, Runions J, Williams LE (2012) HvHMA2, a P1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS One 7:e42640
Miyadate H, Adachi S, Hiraizumi A et al (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199
Morel M, Crouzet J, Gravot A, Auroy P et al (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904
Morman SA, Plumlee GS (2013) The role of airborne mineral dusts in human disease. Aeolian Res 9:203–212
Mostofa MG, Hossain MA, Fujita M, Tran LSP (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433
Mu C, Zhang S, Yu G, Chen N, Li X, Liu H (2013) Overexpression of small heat shock protein LimHSP16. 45 in Arabidopsis enhances tolerance to abiotic stresses. PLoS ONE 8:e82264
Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163
Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta 1763:609–620
Oomen RJ, Wu J, Lelievre F et al (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650
Oono Y, Yazawa T, Kawahara Y et al (2014) Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice. PLoS ONE 9(5):e96946
Oono Y, Yazawa T, Kanamori H et al (2016) Genome-wide transcriptome analysis of cadmium stress in rice. BioMed Res Int 2016:9739505
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
Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728
Ou X, Zhang Y, Xu C, Lin X et al (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE 7(9):e41143
Pan W, Shen J, Zheng Z et al (2018) Overexpression of the Tibetan Plateau annual wild barley (Hordeum spontaneum) HsCIPKs enhances rice tolerance to heavy metal toxicities and other abiotic stresses. Rice 11:51
Pandey R, Muller A, Napoli CA et al (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30:5036–5055
Park CJ, Seo YS (2015) Heat Shock Proteins: A review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333
Park EJ, Jeknic Z, Pino MT, Murata N, Chen TH (2007) Glycine betaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005
Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M et al (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288
Pätsikkä E, Kairavuo M, Šeršen F, Aro EM, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367
Paunov M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V (2018) Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int J Mol Sci 19:787
Peng JS, Gong JM (2014) Vacuolar sequestration capacity and long-distance metal transport in plants. Front Plant Sci 5:19
Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci U S A 98:9995–10000
Pirselova B, Mistrikova V, Libantova J, Moravcikova J, Matusikova I (2012) Study on metal-triggered callose deposition in roots of maize and soybean. Biologia 67:698–705
Pittman JK, Hirschi KD (2016) CAX-ing a wide net: Cation/H(+) transporters in metal remediation and abiotic stress signaling. Plant Biol 18:741–749
Pochodylo AL, Aristilde L (2017) Molecular dynamics of stability and structures in phytochelatin complexes with Zn, Cu, Fe, Mg, and Ca: implications for metal detoxification. Environ Chem Lett 1–6
Pokholok DK, Harbison CT, Levine S et al (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527
Pomponi M, Censi V, Di Girolamo V et al (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190
Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants, In: Heavy Metal Stress in Plants, Springer, pp 121–147
Rao KP, Vani G, Kumar K, Wankhede DP, Misra M, Gupta M et al (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82
Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479
Rono JK, Le Wang L, Wu XC et al (2021) Identification of a new function of metallothionein-like gene OsMT1e for cadmium detoxification and potential phytoremediation. Chemosphere 265:129136
Saher NU, Siddiqui AS (2016) Comparison of heavy metal contamination during the last decade along the coastal sediment of Pakistan: multiple pollution indices approach. Mar Pollut Bull 105:403–410
Samardakiewicz S, Wozny A (2005) Cell division in Lemna minor roots treated with lead. Aquat Bot 83:289–295
Samardakiewicz S, Krzesłowska M, Bilski H, Bartosiewicz R, Wozny A (2012) Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma 249:347–351
Sandeep G, Vijayalatha KR, Anitha T (2019) Heavy metals and its impact in vegetable crops. Int J Chem Stud 7:1612–1621
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167
Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021
Satoh-Nagasawa N, Mori M, Nakazawa N et al (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224
Schellingen K, Van DerStraeten D, Van denBussche F, Prinsen E, Remans T, Vangronsveld J et al (2014) Cadmium-induced ethylene production and responses in Arabidopsis thaliana relyon ACS2 and ACS6 gene expression. BMC Plant Biol 14:214
Schellingen K, Van Der Straeten D, Remans T, Loix C, Vangronsveld J, Cuypers A (2015) Ethylene biosynthesis is involved in the early oxidative challenge induced by moderate Cd exposure in Arabidopsis thaliana. Environ Exp Bot 117:1–11
Schreck E, Laplanche C, Guédard ML, Bessoule JJ, Austruy A, Xiong T, Foucault Y, Dumat C (2013) Influence of fine process particles enriched with metals and metalloids on Lactuca sativa L. leaf fatty acid composition following air and/or soil plant field exposure. Environ Pollut 179:242–249
Shahid M, Xiong T, Castrec Rouelle M, Leveque T, Dumat C (2013) Water extraction kinetics of metals, arsenic and dissolved organic carbon from industrial contaminated poplar leaves. J Environ Sci 25:2451–2459
Shahid M, Pourrut B, Dumat C et al (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44
Shahid M, Dumat C, Khalid S et al (2017) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard Mater 325:36–58
Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. In: KR Hakeem (Ed) Crop Production and Global Environmental Issues SE −1, Springer International Publishing, pp 1–25
Sheikh AH, Badmi R, Jalmi SK, Wankhede DP, Singh P, Sinha AK (2013) Interaction between two rice mitogen activated protein kinases and its possible role in plant defense. BMC Plant Biol 13:121
Shen H, Hou N, Schlicht M, Wan Y, Mancuso S, Baluska F (2008) Aluminium toxicity targets PIN2 in Arabidopsis root apices: effects on PIN2 endocytosis, vesicular recycling, and polar auxin transport. Chin Sci Bull 53:2480–2487
Shen GM, Du QZ, Wang JX (2012) Involvement of plasma membrane Ca2+/H+ antiporter in Cd2+ tolerance. Rice Sci 19:161–165
Shen JQ, Zheng ZZ, Pan WH, Pan JW (2014) Functions and action mechanisms of CBL-CIPK signaling system in plants. Plant Physiol J 50:641–650
Sheoran V, Sheoran AS, Poonia P (2009) Phytomining: a review. Miner Eng 22:1007–1019
Shim D, Kim S, Choi YI et al (2013) Transgenic poplar trees expressing yeast cadmium factor 1 exhibit the characteristics necessary for the phytoremediation of mine tailing soil. Chemosphere 904:1478–1486
Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM (2012) Effect of calcium and potassium on antioxidant system of Viciafaba L. under cadmium stress. Int J Mol Sci 13:6604–6619
Siemianowski O, Barabasz A, Kendziorek M, Ruszczyńska A, Bulska E, Williams LE, Antosiewicz DM (2014) AtHMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J Exp Bot 65:1125–1139
Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Singh P, Mohanta TK, Sinha AK (2015) Unraveling the intricate nexus of molecular mechanisms governing rice root development: OsMPK3/6 and auxin–cytokinin interplay. PLoS ONE 10:e0123620
Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203
Solis EG, Taylor NJ, Siritunga D, Stevens W, Schachtman DP (2015) Overexpression of the transporters AtZIP1 and AtMTP1 in cassava changes zinc accumulation and partitioning. Front Plant Sci 6:492
Song WY, Sohn EJ, Martinoia E et al (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919
Song W, Park J, Mendoza-Cozatl D et al (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci U S A 107:21187–21192
Souza LA, Piotto FA, Nogueirol RC, Azevedo RA (2013) Use of non-hyperaccumulator plant species for the phytoextraction of heavy metals using chelating agents. Scientia Agricola 70:290–295
Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251:1047–1065
Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey RS (2015) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252:959–975
Steinhorst L, Kudla J (2014) Signaling in cells and organisms–calcium holds the line. Curr Opin Plant Biol 22:14–21
Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61:347–356
Sun N, Liu M, Zhang W, Yang W, Bei X, Ma H, Qiao F, Qi X (2015) Bean metal-responsive element-binding transcription factor confers cadmium resistance in tobacco. Plant Physiol 167:1136–1148
Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN et al (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1gene confer Pb2+ tolerance. Plant J 24:533–542
Suzuki N, Koizumi N, Sano H (2001) Screening of cadmium responsive genes in Arabidopsis thaliana. Plant Cell Environ 2:1177–1188
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S et al (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012a) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK et al (2012b) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948–1957
Takahashi R, Ishimaru Y, Shimo H et al (2014) From laboratory to field: OsNRAMP5-knockdown rice is a promising candidate for Cd phytoremediation in paddy fields. PLoS ONE 9(6):e98816
Tang L, Mao B, Li Y et al (2017a) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:1–12
Tang Z, Cai H, Li J et al (2017b) Allelic variation of NtNramp5 associated with cultivar variation in cadmium accumulation in tobacco. Plant Cell Physiol 58:1583–1593
Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97:4991–4996
Thomine S, Lelièvre F, Debarbieux E, Schroeder JI (2003) AtNRAMP3, a multi-specific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695
Tounsi S, Feki K, Kamoun Y et al (2019) Highlight on the expression and the function of a novel MnSOD from diploid wheat (T. monococcum) in response to abiotic stress and heavy metal toxicity. Plant Physiol Biochem 142:384–394
Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, Clemencia Zambrano M et al (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862
Ullah I, Wang Y, Eide DJ, Dunwell JM (2018) Evolution, and functional analysis of natural resistance-associated macrophage proteins (NRAMPs)from Theobroma cacao and their role in cadmium accumulation. Sci Rep 8:14412
Uzu G, Sauvain JJ, Baeza-Squiban A et al (2011) In vitro assessment of the pulmonary toxicity and gastric availability of leadrich particles from a lead recycling plant. Environ Sci Technol 45:7888–7895
Vacchina V, Mari S, Czernic P, Marques L, Pianelli K, Schaumloffel D, Lebrun M, Lobinski R (2003) Speciation of nickel in a hyperaccumulating plant by high performance liquid chromatography-inductively coupled plasma mass spectrometry and electrospray MS/MS assisted by cloning using yeast complementation. Anal Chem 75:2740–2745
Van de Mortel JE, Almar Villanueva L, Schat H et al (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147
Van de Mortel JE, Schat H, Moerland PD et al (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmiumin Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324
Van der Does D, Leon-Reyes A, Koornneef A et al (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761
Van der Zaal BJ, Neuteboom LW et al (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055
Vassilev A, Nikolova A, Koleva L, Lidon F (2011) Effects of excess Zn on growth and photosynthetic performance of young bean plants. J Phytol 3:58–62
Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655
Verret F, Gravot A, Auroy P et al (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312
Vert G, Barberon M, Zelazny E, Séguéla M, Briat JF, Curie C (2009) Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229:1171–1179
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Wang S, Ren X, Huang B, Wang G, Zhou P, An Y (2016) Aluminium induced reduction of plant growth in alfalfa (Medicago sativa) is mediated by interrupting auxin transport and accumulation in roots. Sci Rep 6:30079
Wang C, Wang J, Wang X, Xia Y, Chen C, Shen Z, Chen Y (2017) Proteomic analysis on roots of Oenothera glazioviana under copper-stress conditions. Sci Rep 7:1058
Wanke D, Kolukisaoglu HU (2010) An update on the ABCC transporter family in plants: many genes, many proteins, but how many functions? Plant Biol 1:15–25
Wankhede DP, Kumar K, Singh P, Sinha AK (2013) Involvement of mitogen activated protein kinase kinase 6 in UV induced transcripts accumulation of genes in phytoalexin biosynthesis in rice. Rice 6:35
Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis helleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281
Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+- hyper-tolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963
Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2010) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103
Williams LE, Mills RF (2005) P(1B-) ATPases-an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502
Wojas S, Clemens S, Hennig J et al (2008) Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. J Exp Bot 59(8):2205–2219
Wojas S, Hennig J, Plaza S et al (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Poll 157:2781–2789
Wojas S, Ruszczyńska A, Bulska E, Clemens S, Antosiewicz DM (2010) The role of subcellular distribution of cadmium and phytochelatins in the generation of distinct phenotypes of AtPCS1- and CePCS3-expressing tobacco. J Plant Physiol 167:981–988
Wojcik P (2004) Uptake of mineral nutrients from foliar fertilization. J Fruit Ornamental Plant Res 12
Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78
Wu H, Chen C, Du J, Liu H et al (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhance cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800
Wycisk K, Kim EJ, Schroeder JI, Krämer U (2004) Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett 57:128–134
Xia Y, Qi Y, Yuan Y, Wang G, Cui J, Chen Y, Zhang H, Shen Z (2012) Overexpression of Elsholtzia haichowensis metallothionein 1 (EhMT1) in tobacco plants enhances copper tolerance and accumulation in root cytoplasm and decreases hydrogen peroxide production. J Hazard Mater 233:65–71
Xie K, Chen J, Wang Q, Yang Y (2014) Direct phosphorylation and activation of a mitogen-activated protein kinase by a calcium-dependent protein kinase in rice. Plant Cell 26:3077–3089
Xu W, Shi W, Liu F, Ueda A, Takabe T (2008) Enhanced zinc and cadmium tolerance and accumulation in transgenic Arabidopsis plants constitutively overexpressing a barely gene (HvAPX1) that encodes a peroxisomal ascorbate peroxidase. Botany 86:6
Xu H, Xu W, Xi H, Ma W, He Z, Ma M (2013) The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress-cell death signalling pathway in tobacco cells. J Plant Physiol 170:1434–1441
Yang H, Zhang XY, Wang G (2004) Effects of heavy metals on stomatal movements in broad bean leaves. Russian J Plant Physiol 51:464–468
Yang J, Wang Y, Liu G, Yang C, Li C (2011) Tamarix hispida metallothionein-like ThMT3, a reactive oxygen species scavenger, increases tolerance against Cd2+, Zn2+, Cu2+, and NaCl in transgenic yeast. Mol Biol Rep 38:567–1574
Yang Y, Zhang L, Huang X et al (2020) Response of photosynthesis to different concentrations of heavy metals in Davidiainvolucrate. PLoS One 15(3):e0228563
Yeh CM, Chien PS, Huang HJ (2007) Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671
Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795
Yuan HM, Huang X (2016) Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signaling in Arabidopsis. Plant Cell Environ 39:120–135
Zanella L, Fattorini L, Brunetti P et al (2016) Overexpression of AtPCS1 in tobacco increases arsenic and arsenic plus cadmium accumulation and detoxification. Planta 243:605–622
Zeng H, Xu L, Singh A et al (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci 6:600
Zeng H, Zhang X, Ding M, Zhang X, Zhu Y (2019) Transcriptome profiles of soybean leaves and roots in response to zinc deficiency. Physiol Plant 167:330–351
Zhang GB, Yi HY, Gong JM (2014a) The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–3998
Zhang J, Zhang M, Tian S, Lu L, Shohag MJI et al (2014) Metallothionein 2 (SaMT2) from Sedum alfredii Hance confers increased Cd tolerance and accumulation in yeast and tobacco. PLoS One 9(7):e102750
Zhang M, Zhang J, Lu LL, Zhu ZQ, Yang XE (2016) Functional analysis of CAX2-like transporters isolated from two ecotypes of Sedum alfredii. Biol Plantarum 60:37–47
Zhang H, Lv S, Xu H et al (2017) H2O2 is involved in the metallothionein-mediated rice tolerance to copper and cadmium toxicity. Int J Mol Sci 18:2083
Zhang C, Lu W, Yang Y, Shen Z, Ma JF, Zheng L (2018a) OsYSL16 is required for preferential Cu distribution to floral organs in rice. Plant Cell Physiol 59:2039–2051
Zhang X, Rui H, Zhang F, Hu Z, Xia Y, Shen Z (2018b) Overexpression of a functional Vicia sativa PCS1 homolog increases cadmium tolerance and phytochelatins synthesis in Arabidopsis. Front Plant Sci 9:107
Zhao L, Sun YL, Cui SX et al (2011) Cd-induced changes in leaf proteome of the hyperaccumulator plant Phytolacca americana. Chemosphere 85:56–66
Zhao FY, Hu F, Zhang SY et al (2013) MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environ Sci Pollut Res Int 20:5449–5460
Zhao FY, Wang K, Zhang SY, Ren J, Liu T, Wang X (2014a) Crosstalk between ABA, auxin, MAPK signaling, and the cell cycle in cadmium-stressed rice seedlings. Acta Physiol Plant 36:1879–1892
Zhao L, Wang P, Hou H, Zhang H et al (2014) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS ONE 9(8):e106070
Zhu Z, An F, Feng Y, Li P et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci U S A 108:12539–12544
Zou J, Wang G, Ji J, Wang J, Wu H, Ou Y, Li B (2017) Transcriptional, physiological and cytological analysis validated the roles of some key genes linked Cd stress in Salix matsudana Koidz. Environ Exp Bot 134:116–129
Funding
This work was supported through funding by the Ministry of Higher Education and Scientific Research of Tunisia.
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K.F., H.M., and F.B. conceived and designed the content of the review. M.M. and H.M. proposed valuable ideas and opinions. K.F. and S.T. wrote the manuscript and prepared the figure photos. All authors read and approved the manuscript.
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Feki, K., Tounsi, S., Mrabet, M. et al. Recent advances in physiological and molecular mechanisms of heavy metal accumulation in plants. Environ Sci Pollut Res 28, 64967–64986 (2021). https://doi.org/10.1007/s11356-021-16805-y
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DOI: https://doi.org/10.1007/s11356-021-16805-y