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Genetic engineering of plants for phytoremediation: advances and challenges

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Abstract

Heavy metal and metalloid contamination of the environment due to natural processes, industrialization, and anthropogenic activities pose a serious problem, threatening the health of millions of people exposed to drinking water and crop plants grown in contaminated areas. The traditional remediation method often includes the removal of pollutants physically and their disposal, an expensive, non-specific process that renders the soil unfit for cultivation and other usages. Phytoremediation is a successful approach for various heavy metal and metalloid decontamination. Multiple biotechnological tools, including genetic alteration of plants, can be employed to strengthen the phytoremediation capacity. Plant genetic engineering for phytoremediation can be an effective approach to exploit potential genes involved in metal uptake, translocation, reduction, complexation, vacuolar sequestration, and volatilization. However, one needs to understand the mechanism of increased accumulation of heavy metals in hyperaccumulators and translate the findings into high biomass crop plants for sustainable cleansing of the environment. This review will discuss various genetic engineering approaches for intensifying the phytoremediation capacity of plants for heavy metal and metalloids (Cd, Pb, Cr, As, Se and Hg), highlighting the recent advances and their limitations. We will also highlight the molecular understanding of various regulatory and signaling molecules and their utilization in improving the phytoremediation potential of plants. The review will also evaluate various limitations and challenges of the genetic engineering approaches.

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Abbreviations

Cd:

cadmium

Cr:

chromium

Pb:

lead

Hg:

mercury

Se:

selenium

As:

arsenic

HMs:

heavy metals

WT:

wild type

GSH:

glutathione

MTs:

metallothioneins

PCs:

phytochelatins

NO:

nitric oxide

APR2:

adenosine 5’-phosphosulfate reductase 2

Hb:

hemoglobin

LMWOA:

low molecular weight organic and amino acid

AtCNGC1:

Arabidopsis cyclic nucleotide-gated ion channel

γ-ECS:

γ-glutamyl cysteine synthetase

ROS:

reactive oxygen species

References

  • Agarwal P, Giri B, Rani R (2020) Unravelling the role of rhizospheric plant-microbe synergy in phytoremediation: A genomic perspective. Curr Genomics 21:334–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd_Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

  • Ali H, Khan E, Sajad M (2013) Phytoremediation of heavy metals-Concepts and applications. Chemosphere 91:869–881

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Arif MS, Yasmeen T, Abbas Z, Ali S, Rizwan M, Aljarba NH, Alkahtani S, Abdel-Daim MM (2021) Role of exogenous and endogenous hydrogen sulfide (H2S) on functional traits of plants under heavy metal stresses: A recent perspective. Front Plant Sci 11:2063

    Article  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  CAS  PubMed  Google Scholar 

  • Auguy F, Fahr M, Moulin P, Brugel A, Laplaze L, Mzibri ME, Filali-Maltouf A, Doumas P, Smouni A (2013) Lead tolerance and accumulation in Hirschfeldia incana, a mediterranean Brassicaceae from metalliferous mine spoils. PLoS ONE 8:e61932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayyappan D, Ravindran KC (2014) Phytoextraction of heavy metals and ions from tannery effluent using Suaeda monoica Forsk. with reference to morphology and anatomical characters. Int J Curr 2:292–304

    CAS  Google Scholar 

  • Ayyappan D, Sathiyaraj G, Ravindran K (2015) Phytoextraction of heavy metals by Sesuvium portulacastruml. a salt marsh halophyte from tannery effluent. Int J Phytoremediation 18:453–459

    Article  Google Scholar 

  • Bahmani R, Kim D, Na J, Hwang S (2019) Expression of the tobacco Non-symbiotic class 1 hemoglobin gene Hb1 reduces cadmium levels by modulating Cd transporter expression through decreasing nitric oxide and ROS level in Arabidopsis. Front Plant Sci 10:201

    Article  PubMed  PubMed Central  Google Scholar 

  • Baliardini C, Meyer, Salis P, Saumitou-Laprade P, Verbruggen N (2015) CATION EXCHANGER1 cosegregates with cadmium tolerance in the metal myperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis Spp. Plant Physiol 169:549–559

    Article  PubMed  PubMed Central  Google Scholar 

  • Basharat Z, Novo L, Yasmin A (2018) Genome editing weds CRISPR: what is in it for phytoremediation? Plants 7:51

  • Basu S, Rabara R, Negi S, Shukla P (2018) Engineering PGPMOs through gene editing and systems biology: A solution for phytoremediation? Trends Biotechnol 36:499–510

    Article  CAS  PubMed  Google Scholar 

  • Bernardino CA, Mahler CF, Alvarenga P, Castro PM, da Silva EF, Novo LA (2019) Recent advances in phytoremediation of soil contaminated by industrial waste: A road map to a safer environment. In: Saxena G, Bharagava RN (eds) Bioremediation of Industrial Waste for Environmental Safety. Springer Singapore, pp 207–221

  • Bridges C, Zalups R (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204:274–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunetti P, Zanella L, Proia A, De Paolis A, Falasca G, Altamura MM, Sanita di Toppi L, Costantino P, Cardarelli M (2011) Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. J Exp Bot 62:5509–5519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bücker-Neto L, Paiva ALS, Machado RD, Arenhart RA, Margis-Pinheiro M (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386

    Article  PubMed  PubMed Central  Google Scholar 

  • Callahan DL, Hare DJ, Bishop DP, Doble PA, Roessner U (2016) Elemental imaging of leaves from the metal hyperaccumulating plant Noccaea caerulescens shows different spatial distribution of Ni, Zn and Cd. RSC Adv 6:2337–2344

    Article  CAS  Google Scholar 

  • Cao Y, Feng H, Sun D, Xu G, Rathinasabapathi B, Chen Y, Ma LQ (2019) Heterologous expression of Pteris vittata phosphate transporter PvPht1;3 enhances arsenic translocation to and accumulation in tobacco shoots. Environ Sci Technol 53:10636–10644

    Article  CAS  PubMed  Google Scholar 

  • Chaudhry H, Nisar N, Mehmood S, Iqbal M, Nazir A, Yasir M (2020) Indian Mustard Brassica juncea efficiency for the accumulation, tolerance and translocation of zinc from metal contaminated soil. Biocatal Agric Biotechnol 23:101489

    Article  Google Scholar 

  • Che D, Meagher RB, Heaton AC, Lima A, Rugh CL, Merkle SA (2003) Expression of mercuric ion reductase in Eastern cottonwood (Populus deltoides) confers mercuric ion reduction and resistance. Plant Biotechnol 1:311–319

    Article  CAS  Google Scholar 

  • Chen J, Yang L, Gu J, Bai X, Ren Y, Fan T, Han Y, Jiang L, Xiao F, Liu Y, Cao S (2014) MAN3 gene regulates cadmium tolerance through the glutathione dependent pathway in Arabidopsis thaliana. New Phytol 205:570–582

    Article  PubMed  Google Scholar 

  • Chen K, Chen L, Fan J, Fu J (2013a) Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. Photosynth Res 116:21–31

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Han X, Fang J, Lu Z, Qiu W, Liu M, Sang J, Jiang J, Zhuo R (2017a) Sedum alfredii SaNramp6 metal transporter contributes to cadmium accumulation in transgenic Arabidopsis thaliana. Sci Rep 7:13318

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Xu W, Shen H, Yan H, Xu W, He Z, Ma M (2013b) Engineering arsenic tolerance and hyperaccumulation in plants for phytoremediation by a PvACR3 transgenic approach. Environ Sci Technol 47:9355–9362

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zheng Y, Ding C, Ren X, Yuan J, Sun F, Li Y (2017b) Integrated metagenomics and molecular ecological network analysis of bacterial community composition during the phytoremediation of cadmium-contaminated soils by bioenergy crops. Ecotoxicol Environ Saf 145:111–118

    Article  CAS  PubMed  Google Scholar 

  • Choudhury F, Rivero R, Blumwald E, Mittler R (2016) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  PubMed  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Palmgren M, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  PubMed  Google Scholar 

  • Cobbett C (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosio C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775

    Article  CAS  PubMed  Google Scholar 

  • Dai J, Balish R, Meagher R, Merkle S (2009) Development of transgenic hybrid sweetgum (Liquidambar styraciflua × L. formosana) expressing γ-glutamylcysteine synthetase or mercuric reductase for phytoremediation of mercury pollution. New For (Dordr) 38:35–52

    Google Scholar 

  • DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions: state of the art and innovation in phytoremediation. Int J Mol Sci 20:3412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalvi AA, Bhalerao SA (2013) Response of plants towards heavy metal toxicity: an overview of avoidance, tolerance and uptake mechanism. Ann Plant Sci 2:362–368

    Google Scholar 

  • Danh L, Truong P, Mammucari R, Foster N (2013) A critical review of the arsenic uptake mechanisms and phytoremediation potential of Pteris vittata. Int J Phytoremediation 16:429–453

    Article  Google Scholar 

  • Das N, Bhattacharya S, Maiti M (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

    Article  CAS  PubMed  Google Scholar 

  • Deng F, Zeng F, Chen G, Feng X, Riaz A, Wu X, Gao W, Wu F, Holford P, Chen ZH (2021) Metalloid hazards: From plant molecular evolution to mitigation strategies. J Hazard Mater 409:124495

    Article  CAS  PubMed  Google Scholar 

  • Deng TH, Tang YT, van der Ent A, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45

    Article  CAS  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    Article  CAS  PubMed  Google Scholar 

  • Dhankher O, Pilon-Smits E, Meagher R, Doty S (2012) Biotechnological approaches for phytoremediation. In: Altman A, Hasegawa P (eds) Plant Biotechnology and Agriculture, 1st edn. Academic Press, Cambridge, pp 309–328

    Chapter  Google Scholar 

  • Dhankher OP, Shasti NA, Rosen BP, Fuhrmann M, Meagher RB (2003) Increased cadmium tolerance and accumulation by plants expressing bacterial arsenate reductase. New Phytol 159:431–441

    Article  CAS  PubMed  Google Scholar 

  • Doty S (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    Article  CAS  PubMed  Google Scholar 

  • Evangelou M, Ebel M, Schaeffer A (2006) Evaluation of the effect of small organic acids on phytoextraction of Cu and Pb from soil with tobacco Nicotiana tobacum. Chemosphere 63:996–1004

    Article  CAS  PubMed  Google Scholar 

  • Fan T, Yang L, Wu X, Ni J, Jiang H, Zhang QA, Fang L, Sheng Y, Ren Y, Cao S (2016) The PSE1gene modulates lead tolerance in Arabidopsis. J Exp Bot 67:4685–4695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan W, Guo Q, Liu C, Liu X, Zhang M, Long D, Xiang Z, Zhao A (2018) Two mulberry phytochelatin synthase genes confer zinc/cadmium tolerance and accumulation in transgenic Arabidopsis and tobacco. Gene 645:95–104

    Article  CAS  PubMed  Google Scholar 

  • Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis Book 11:e0166

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu JW, Liu X, Han YH, Mei H, Cao Y, de Oliveira LM, Liu Y, Rathinasabapathi B, Chen Y, Ma LQ (2017) Arsenic-hyperaccumulator Pteris vittata efficiently solubilized phosphate rock to sustain plant growth and As uptake. J Hazard Mater 330:68–75

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Mason AS, Zhang Y, Lin B, Xiao M, Fu D, Yu H (2019) MicroRNA-mRNA expression profiles and their potential role in cadmium stress response in Brassica napus. BMC Plant Biol 19:1–20

    Article  Google Scholar 

  • Fulcher N, Riha K (2016) Using centromere mediated genome elimination to elucidate the functional redundancy of candidate telomere binding proteins in Arabidopsis thaliana. Front Genet 6:349

    Article  PubMed  PubMed Central  Google Scholar 

  • Gasic K, Korban S (2007) Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol 64:361–369

    Article  CAS  PubMed  Google Scholar 

  • Gisbert C, Ros R, De Haro A, Walker DJ, Bernal MP, Serrano R, Navarro-Aviñó J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303:440–445

    Article  CAS  PubMed  Google Scholar 

  • Goliński P, Mleczek M, Magdziak Z, Gąsecka M, Borowiak K, Dąbrowski J, Kaczmarek Z, Rutkowski P (2015) Efficiency of Zn phytoextraction, biomass yield and formation of low-molecular-weight organic acids in S. rubens- a hydroponic experiment. Chem Ecol 31:345–364

    Article  Google Scholar 

  • Gomi K, Ogawa D, Katou S, Kamada H, Nakajima N, Saji H, Soyano T, Sasabe M, Machida Y, Mitsuhara I, Ohashi Y (2005) A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol 46:1902–1914

    Article  CAS  PubMed  Google Scholar 

  • Grill E, Winnacker E, Zenk M (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026

    Article  CAS  PubMed  Google Scholar 

  • Guo Q, Meng L, Humphreys MW, Scullion J, Mur LA (2017) Expression of FlHMA3, a P1B2 -ATPase from Festulolium loliaceum, correlates with response to cadmium stress. Plant Physiol Biochem 112:270–277

    Article  CAS  PubMed  Google Scholar 

  • Gupta D, Huang H, Corpas F (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20:2150–2161

    Article  CAS  Google Scholar 

  • Gupta M, Sharma P, Sarin N, Sinha A (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74:1201–1208

    Article  CAS  PubMed  Google Scholar 

  • Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  CAS  PubMed  Google Scholar 

  • Haque S (2010) Transgenic tobacco plant expressing environmental E. coli merA gene for enhanced volatilization of ionic mercury. J Microbiol Biotechnol 20:917–924

    Article  PubMed  Google Scholar 

  • Hasegawa I, Terada E, Sunairi M, Wakita H, Shinmachi F, Noguchi A, Nakajima M, Yazaki J (1997) Genetic improvement of heavy metal tolerance in plants by transfer of the yeast metallothionein gene (CUP1). Plant Soil 196:277–281

    Article  CAS  Google Scholar 

  • He J, Li H, Ma C, Zhang Y, Polle A, Rennenberg H, Cheng X, Luo ZB (2014) Overexpression of bacterial γ-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254

    Article  PubMed  Google Scholar 

  • He YK, Sun JG, Feng XZ, Czakó M, Márton L (2001) Differential mercury volatilization by tobacco organs expressing a modified bacterial merA gene. Cell Res 11:231–236

    Article  CAS  PubMed  Google Scholar 

  • Heaton AC, Rugh CL, Kim T, Wang NJ, Meagher RB (2003) Toward detoxifying mercury-polluted aquatic sediments with rice genetically engineered for mercury resistance. Environ Toxicol Chem 22:2940

    Article  CAS  PubMed  Google Scholar 

  • Heaton A, Rugh C, Wang N, Meagher R (2005) Physiological responses of transgenic merA-tobacco (Nicotiana tobacum) to foliar and root mercury exposure. Water Air Soil Pollut 161:137–155

    Article  CAS  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LS (2016) Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance. Front Plant Sci 7:1341

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh JL, Chen CY, Chiu MH, Chein MF, Chang JS, Endo G, Huang CC (2009) Expressing a bacterial mercuric ion binding protein in plant for phytoremediation of heavy metals. J Hazard Mater 161:920–925

    Article  CAS  PubMed  Google Scholar 

  • Hu YF, Zhou G, Na XF, Yang L, Nan WB, Liu X, Zhang YQ, Li JL, Bi YR (2013) Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. J Plant Physiol 170:965–975

    Article  CAS  PubMed  Google Scholar 

  • Huang HJ, Fu SF, Tai YH, Chou WC, Huang DD (2002) Expression of Oryza sativa MAP kinase gene is developmentally regulated and stress-responsive. Physiol Plant 114:572–580

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390

    Article  CAS  PubMed  Google Scholar 

  • Ivanova LA, Ronzhina DA, Ivanov LA, Stroukova LV, Peuke AD, Rennenberg H (2011) Over-expression of GSH1 in the cytosol affects the photosynthetic apparatus and improves the performance of transgenic poplars on heavy metal-contaminated soil. Plant Biol 13:649–659

    Article  CAS  PubMed  Google Scholar 

  • Jadia CD, Fulekar MH (2009) Phytoremediation of heavy metals: Recent techniques. Afr J Biotechnol 8:921–928

    CAS  Google Scholar 

  • Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sharma D, Sinha AK (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci 9:12

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kärenlampi S, Schat H, Vangronsveld J, Verkleij JA, van der Lelie D, Mergeay M, Tervahauta AI (2000) Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ Pollut 107:225–231

    Article  PubMed  Google Scholar 

  • Karle SB, Guru A, Dwivedi P, Kumar K (2021) Insights into the role of gasotransmitters mediating salt stress responses in plants. J Plant Growth Regul 40:2259–2271

    Article  CAS  Google Scholar 

  • Kaur P, Bali S, Sharma A, Vig AP, Bhardwaj R (2018) Role of earthworms in phytoremediation of cadmium (CD) by modulating the antioxidative potential of Brassica juncea L. Appl Soil Ecol 124:306–316

    Article  Google Scholar 

  • Kaya C (2020) Salicylic acid-induced hydrogen sulphide improves lead stress tolerance in pepper plants by upraising the ascorbate-glutathione cycle. Physiol Plant 173:8–19

    PubMed  Google Scholar 

  • Khator K, Saxena I, Shekhawat G (2020) Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. Biometals 34:15–32

    Article  PubMed  Google Scholar 

  • Khoudi H, Maatar Y, Gouiaa S, Masmoudi K (2012) Transgenic tobacco plants expressing ectopically wheat H+-pyrophosphatase (H+-PPase) gene TaVP1 show enhanced accumulation and tolerance to cadmium. J Plant Physiol 169:98–103

    Article  CAS  PubMed  Google Scholar 

  • Kotrba P, Najmanova J, Macek T, Ruml T, Mackova M (2009) Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotechnol Adv 27:799–810

    Article  CAS  PubMed  Google Scholar 

  • Kovtun Y, Chiu W, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci 97:2940–2945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozhevnikova A, Seregin I, Aarts M, Schat H (2020) Intra-specific variation in zinc, cadmium and nickel hypertolerance and hyperaccumulation capacities in Noccaea caerulescens. Plant Soil 452:479–498

    Article  CAS  Google Scholar 

  • Koźmińska A, Wiszniewska A, Hanus-Fajerska E, Muszyńska E (2018) Recent strategies of increasing metal tolerance and phytoremediation potential using genetic transformation of plants. Plant Biotechnol Rep 12:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi Species. Plant Physiol 122:1343–1354

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar K, Raina SK, Sultan SM (2020) Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. J Plant Biochem Biotechnol 29:700–714

    Article  CAS  Google Scholar 

  • Kumar RM, Ji G, Guo H, Zhao L, Zheng B (2018) Over-expression of a grafting-responsive gene from hickory increases abiotic stress tolerance in Arabidopsis. Plant Cell Rep 37:541–552

    Article  CAS  PubMed  Google Scholar 

  • Küpper H, Jie Zhao F, McGrath S (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–312

    Article  PubMed Central  Google Scholar 

  • Küpper H, Lombi E, Zhao F, McGrath S (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84

  • Leal-Alvarado DA, Estrella-Maldonado H, Sáenz-Carbonell L, Ramírez-Prado JH, Zapata-Pérez O, Santamaría JM (2018) Genes coding for transporters showed a rapid and sharp increase in their expression in response to lead, in the aquatic fern (Salvinia minima Baker). Ecotoxicol Environ Saf 147:1056–1064

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc M, McKinney E, Meagher R, Smith A (2013) Hijacking membrane transporters for arsenic phytoextraction. J Biotechnol 163:1–9

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Roberts S, Morel F (1995) Cadmium: A nutrient for the marine diatom. Thalassiosira weissflogii Limnol Oceanogr 40:1056–1063

    Article  CAS  Google Scholar 

  • Li J, Yue L, Shen Y, Sheng Y, Zhan X, Xu G, Xing B (2017) Phenanthrene-responsive microRNAs and their targets in wheat roots. Chemosphere 186:588–598

    Article  CAS  PubMed  Google Scholar 

  • Li X, Sun D, Feng H, Chen J, Chen Y, Li H, Cao Y, Ma LQ (2020) Efficient arsenate reduction in As-hyperaccumulator Pteris vittata are mediated by novel arsenate reductases PvHAC1 and PvHAC2. J Hazard Mater 399:122895

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Min X, Zhou Z (2016) Hydrogen Sulfide: A signal molecule in plant cross-adaptation. Front Plant Sci 7:1621

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindsay E, Maathuis F (2016) Arabidopsis thaliana NIP7;1 is involved in tissue arsenic distribution and tolerance in response to arsenate. FEBS Lett 590:779–786

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signaling molecule? Plant Cell Environ 36:1607–1616

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Ding S, Zhang A, Hong K, Jiang H, Yang S, Ruan B, Zhang B, Dong G, Guo L, Zeng D (2020) Development of nutritious rice with high zinc/selenium and low cadmium in grains through QTL pyramiding. J Integr Plant Biol 62:349–359

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Yuan JS, Stewart CN Jr (2013) Advanced genetic tools for plant biotechnology. Nat Rev Genet 14:781–793

    Article  CAS  PubMed  Google Scholar 

  • Luo JS, Xiao Y, Yao J, Wu Z, Yang Y, Ismail AM, Zhang Z (2020) Overexpression of a defensin-like gene CAL2 enhances cadmium accumulation in plants. Front Plant Sci 11:217

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo Z, 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

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Natl Acad Sci 105:9931–9935

    Article  CAS  Google Scholar 

  • Martins N, Gonçalves S, Andrade PB, Valentão P, Romano A (2013) Changes on organic acid secretion and accumulation in Plantago almogravensis Franco and Plantago algarbiensis Samp. under aluminum stress. Plant Sci 198:1–6

    Article  CAS  PubMed  Google Scholar 

  • Memon A, Aktoprakligi̇l D, Özdemi̇r A, Vertii A (2001) Heavy Metal Accumulation and Detoxification Mechanisms in Plants. Turk J Botany 25:111–121

    Google Scholar 

  • Memon A, Schröder P (2008) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16:162–175

    Article  Google Scholar 

  • Mesa-Marin J, Pérez-Romero JA, Redondo-Gómez S, Pajuelo E, Rodríguez-Llorente ID, Mateos-Naranjo E (2020) Impact of plant growth promoting bacteria on Salicornia ramosissima ecophysiology and heavy metal phytoremediation capacity in estuarine soils. Front Microbiol 11:2148

    Article  Google Scholar 

  • Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I (2010) OsHMA3, a P1B-type of ATPase affects root to shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199

    Article  PubMed  Google Scholar 

  • Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP (2016) Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front Plant Sci 7:303

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukta R, Khatun M, Nazmul Huda A (2019) Calcium induces phytochelatin accumulation to cope with chromium toxicity in rice (Oryza sativa L.). J Plant Interact 14:295–302

    Article  CAS  Google Scholar 

  • Muthu V, Abbai R, Nallathambi J, Rahman H, Ramasamy S, Kambale R, Thulasinathan T, Ayyenar B, Muthurajan R (2020) Pyramiding QTLs controlling tolerance against drought, salinity, and submergence in rice through marker assisted breeding. PLoS ONE 15:e0227421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muthusaravanan S, Sivarajasekar N, Vivek JS, Paramasivan T, Naushad M, Prakashmaran J, Gayathri V, Al-Duaij OK (2018) Phytoremediation of heavy metals: mechanisms, methods and enhancements. Environ Chem Lett 16:1339–1359

    Article  CAS  Google Scholar 

  • Nabaei M, Amooaghaie R (2019) Melatonin and nitric oxide enhance cadmium tolerance and phytoremediation efficiency in Catharanthus roseus (L.) G. Don. Environ Sci Pollut Res 27:6981–6994

    Article  Google Scholar 

  • Nagata T, Morita H, Akizawa T, Pan-Hou H (2010) Development of a transgenic tobacco plant for phytoremediation of methylmercury pollution. Appl Microbiol Biotechnol 87:781–786

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasternak T, Potters G, Caubergs R, Jansen M (2005) Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J Exp Bot 56:1991–2001

    Article  CAS  PubMed  Google Scholar 

  • Paul B, Snyder S, Kashfi K (2021) Effects of hydrogen sulfide on mitochondrial function and cellular bioenergetics. Redox Biol 38:101772

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1–MKK1/2–MPK4 pathway in ROS signaling. Mol Plant 2:120–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pomponi M, Censi V, Di Girolamo V, De Paolis A, Di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2005) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    Article  PubMed  Google Scholar 

  • Rao KP, Vani G, Kumar K, Wankhede DP, Misra M, Gupta M, Sinha AK (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82

    Article  CAS  PubMed  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  CAS  PubMed  Google Scholar 

  • Raskin I, Smith R, Salt D (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226

    Article  CAS  PubMed  Google Scholar 

  • Reeves RD, Baker AJ, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2017) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407–411

    Article  PubMed  Google Scholar 

  • Renella G, Landi L, Nannipieri P (2004) Degradation of low molecular weight organic acids complexed with heavy metals in soil. Geoderma 122:311–315

    Article  CAS  Google Scholar 

  • Ritchie S, Gilroy S (2000) Abscisic Acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant Physiol 124:693–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+–calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20:600–608

    Article  CAS  Google Scholar 

  • Rono JK, Le Wang L, Wu XC, Cao HW, Zhao YN, Khan IU, Yang ZM (2021) Identification of a new function of metallothionein-like gene OsMT1e for cadmium detoxification and potential phytoremediation. Chemosphere 265:129136

    Article  CAS  PubMed  Google Scholar 

  • Rugh C, Senecoff J, Meagher R, Merkle S (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928

    Article  CAS  PubMed  Google Scholar 

  • Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci 93:3182–3187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz ON, Alvarez D, Torres C, Roman L, Daniell H (2011) Metallothionein expression in chloroplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnol J 9:609–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seregin I, Kozhevnikova A (2020) Low-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation. Photosynth Res 150:51–96

    Article  PubMed  Google Scholar 

  • Shailani A, Joshi R, Singla-Pareek S, Pareek A (2020) Stacking for future: Pyramiding genes to improve drought and salinity tolerance in rice. Physiol Plant 172:1352–1362

    Article  PubMed  Google Scholar 

  • Shan CJ, Zhang SL, Li DF, Zhao YZ, Tian XL, Zhao XL, Wu YX, Wei XY, Liu RQ (2011) Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Physiol Plant 33:2533–2540

    CAS  Google Scholar 

  • Sharma R, Yeh K (2020) The dual benefit of a dominant mutation in Arabidopsis IRON DEFICIENCY TOLERANT1 for iron biofortification and heavy metal phytoremediation. Plant Biotechnol J 18:1200–1210

    Article  CAS  PubMed  Google Scholar 

  • Siemianowski O, Barabasz A, Kendziorek M, Ruszczyńska A, Bulska E, Williams LE, Antosiewicz DM (2014) HMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J Exp Botany 65:1125–1139

  • Singh AP, Dixit G, Kumar A, Mishra S, Singh PK, Dwivedi S, Trivedi PK, Chakrabarty D, Mallick S, Pandey V, Dhankher OP (2016a) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci 6:1272

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016b) Heavy metal tolerance in plants: Role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh V, Singh S, Kumar J, Prasad S (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: Possible involvement of nitric oxide. J Plant Physiol 181:20–29

    Article  CAS  PubMed  Google Scholar 

  • Sinha A, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Feng SJ, Chen J, Zhao WT, Yang ZM (2017) A cadmium stress-responsive gene AtFC1 confers plant tolerance to cadmium toxicity. BMC Plant Biol 17:1–15

    Article  CAS  Google Scholar 

  • Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey R (2014) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252:959–975

    Article  PubMed  Google Scholar 

  • Summers A, Sugarman L (1974) Cell-free mercury(ii)-reducing activity in a plasmid-bearing strain of Escherichia coli.. J Bacteriol Res 119:242–249

    Article  CAS  Google Scholar 

  • Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542

    Article  CAS  PubMed  Google Scholar 

  • Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2018) Phytohormone priming: Regulator for heavy metal stress in plants. J Plant Growth Regul 38:739–752

    Article  Google Scholar 

  • Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948–1957

    Article  CAS  PubMed  Google Scholar 

  • Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X, Shao Y, Pan Y (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:1–12

    Article  Google Scholar 

  • Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011:1–31

    Article  Google Scholar 

  • Thakur S, Choudhary S, Majeed A, Singh A, Bhardwaj P (2019) Insights into the molecular mechanism of arsenic phytoremediation. J Plant Growth Regul 39:532–543

    Article  Google Scholar 

  • Thakur S, Singh L, Wahid ZA, Siddiqui MF, Atnaw SM, Din MF (2016) Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess 188:1–11

    Article  Google Scholar 

  • Thondehaalmath T, Kulaar D, Bondada R, Maruthachalam R (2021) Understanding and exploiting uniparental genome elimination in plants: insights from Arabidopsis thaliana. J Exp Bot 72:4646–4662

    Article  CAS  PubMed  Google Scholar 

  • Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84:63–69

    Article  CAS  PubMed  Google Scholar 

  • Vasudevan R, Gale GA, Schiavon AA, Puzorjov A, Malin J, Gillespie MD, Vavitsas K, Zulkower V, Wang B, Howe CJ, Lea-Smith DJ (2019) CyanoGate: A modular cloning suite for engineering cyanobacteria based on the plant MoClo syntax. Plant Physiol 180:39–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma S, Verma PK, Meher AK, Bansiwal AK, Tripathi RD, Chakrabarty D (2018) A novel fungal arsenic methyltransferase, WaarsM reduces grain arsenic accumulation in transgenic rice (Oryza sativa L.). J Hazard Mater 344:626–634

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896

    Article  CAS  PubMed  Google Scholar 

  • Wojas S, Ruszczyńska A, Bulska E, Wojciechowski M, Antosiewicz DM (2007) Ca2+–dependent plant response to Pb2+ is regulated by LCT1. Environ Pollut 147:584–592

    Article  CAS  PubMed  Google Scholar 

  • Xiao E, Cui J, Sun W, Jiang S, Huang M, Kong D, Wu Q, Xiao T, Sun X, Ning Z (2021) Root microbiome assembly of As hyperaccumulator Pteris vittata and its efficacy in arsenic requisition. Environ Microbiol 23:1959–1971

    Article  CAS  PubMed  Google Scholar 

  • Xie Y, Hu L, Du Z, Sun X, Amombo E, Fan J, Fu J (2014) Effects of cadmium exposure on growth and metabolic profile of bermudagrass [Cynodon dactylon (L.) Pers.]. PLoS ONE 9:e115279

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Wang M, Xu D, Xia Z (2020) The Arabidopsis APR2 positively regulates cadmium tolerance through glutathione-dependent pathway. Ecotoxicol Environ Saf 187:109819

    Article  CAS  PubMed  Google Scholar 

  • Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: A promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan J, Wang P, Wang P, Yang M, Lian X, Tang Z, Huang CF, Salt DE, Zhao FJ (2016) A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ 39:1941–1954

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Kang Y, Liu Y, Shi M, Zhang W, Fan Y, Yao Y, Li H, Qin S (2021) Integrated analysis of miRNA-mRNA regulatory networks of potato (Solanum tuberosum L.) in response to cadmium stress. Ecotoxicol Environ Saf 224:112682

    Article  CAS  PubMed  Google Scholar 

  • Yeh C, Chien P, Huang H (2006) Distinct signaling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671

    Article  Google Scholar 

  • Zanella L, Fattorini L, Brunetti P, Roccotiello E, Cornara L, D’Angeli S, Della Rovere F, Cardarelli M, Barbieri M, di Sanità L, Degola F (2015) Overexpression of AtPCS1 in tobacco increases arsenic and arsenic plus cadmium accumulation and detoxification. Planta 243:605–622

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci 6:600

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Xiao X, Yan G, Hu J, Cheng X, Li L, Li H, Wu X (2018) Association mapping of cadmium-tolerant QTLs in Brassica napus L. and insight into their contributions to phytoremediation. Environ Exp Bot 155:420–428

    Article  CAS  Google Scholar 

  • Zhang J, Zhang M, Shohag M, Islam J, Tian S, Song H, Feng Y, Yang X (2015) Enhanced expression of SaHMA3 plays critical roles in Cd hyperaccumulation and hypertolerance in Cd hyperaccumulator Sedum alfredii Hance. Planta 243:577–589

    Article  PubMed  Google Scholar 

  • Zhen L, Mingying L, Xiaojiao H, Guirong Q, Jing J, Shiyan X, Renying Z (2014) Characterization of a light-harvesting chlorophyll a/b binding protein (LHCB) gene, SaLhcb2, in Sedum alfredii. J Zhejiang Univ Sci B 31:838–846

  • Zhao F, Huang X (2018) Cadmium phytoremediation: Call rice CAL1. Mol Plant 11:640–642

    Article  CAS  PubMed  Google Scholar 

  • Zhu YX, Du WX, Fang XZ, Zhang LL, Jin CW (2020) Knockdown of BTS may provide a new strategy to improve cadmium-phytoremediation efficiency by improving iron status in plants. J Hazard Mater 384:121473

    Article  CAS  PubMed  Google Scholar 

  • Zulfiqar F, Hancock J (2020) Hydrogen sulfide in horticulture: Emerging roles in the era of climate change. Plant Physiol Biochem 155:667–675

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors thank BITS-Pilani, K. K. Birla Goa Campus, for providing the necessary support.

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  1. Department of Biological Sciences, Birla Institute of Technology and Science Pilani, K. K. Birla Goa Campus, Goa, 403726, India

    Kundan Kumar, Akshay Shinde, Varad Aeron & Aanchal Verma

  2. Department of Biotechnology, R V College of Engineering, Bengaluru, 560059, Karnataka, India

    Naseera Sayed Arif

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Kumar, K., Shinde, A., Aeron, V. et al. Genetic engineering of plants for phytoremediation: advances and challenges. J. Plant Biochem. Biotechnol. 32, 12–30 (2023). https://doi.org/10.1007/s13562-022-00776-3

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