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Physiological responses, tolerance, and remediation strategies in plants exposed to metalloids

  • Emerging Trends in Biotechnology for Sustainable Development and Pollution Prevention
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Abstract

Metalloids are a subset of particular concern to risk assessors and toxicologists because of their well-documented potential hazards to plant system. Most of the metalloids are major environmental contaminants which affect crop productivity when present in high concentrations in soil. Metalloids are coupled with carrier proteins of the plasma membrane and translocated to various organs causing changes in key metabolic processes, damages cell biomolecules, and finally inhibit its growth. Phytoremediation-based approaches help in understanding the molecular and biochemical mechanisms for prerequisite recombinant genetic approaches. Recent advancements in proteomics and plant genomics help in understanding the role of transcription factors, metabolites, and genes in plant system which confers metal tolerance. The present review summarizes our current status of knowledge in this direction related to various physiological responses, detoxification mechanisms, and remediation strategies of metalloids in crop plants in relation to plant-metalloid tolerance. Further, the role of various transcription factors and miRNAs in conferring metal tolerance is also briefed. Hence, the present review mainly focused on the alterations in the physiological activities of plants due to metalloid toxicity and the various mechanisms which get activated inside the plants to mitigate their toxic effects.

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References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi N, Khan M, Amjad M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Ram M (2010) Boron induced oxidative stress, antioxidant defence response and changes in artemisinin content in Artemisia annua L. J Agron Crop Sci 196(6):423–430

    Article  CAS  Google Scholar 

  • Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandhari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H (2011) Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biol Trace Elem Res 140(3):354–367

    Article  CAS  Google Scholar 

  • Ahmad S, Tripathy DB, Mishra A (2011) Sustainable nanomaterials. Encycl Inorg Bioinorg Chem:1–15

  • Aiman U, Mahmood A, Waheed S, Malik RN (2016) Enrichment, geo-accumulation and risk surveillance of toxic metals for different environmental compartments from Mehmood Booti dumping site, Lahore city, Pakistan. Chemosphere 144:2229–2237

    Article  CAS  Google Scholar 

  • Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Biotechnol 3:71–90

    Article  CAS  Google Scholar 

  • Alloway BJ (Ed.) (2012) heavy metals in soils: trace metals and metalloids in soils and their bioavailability (Vol. 22). Springer, Dordrecht, Heidelberg. New York, London

  • Alloway BJ (Ed.) (2013) Sources of heavy metals and metalloids in soils. In: Heavy metals in soils. Springer, Dordrecht. pp. 11–50

  • Amir R, Taufiq S, Noor N, Nauman I, Munir F, Keyani R, Tahir AT (2018) Stress signaling under metal and metalloid toxicity. In: Plants under metal and metalloid stress. Springer, Singapore. pp. 149–184

  • Artyszak A (2018) Effect of silicon fertilization on crop yield quantity and quality—A literature review in Europe. Plants 7(3):54

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E, Ahmad I, Tuteja R, Tuteja N (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251:1265–1283

    Article  CAS  Google Scholar 

  • Aquea F, Federici F, Moscoso C, Vega A, Jullian P, Haseloff JIM, Arce-Johnson PA (2012) A molecular framework for the inhibition of Arabidopsis root growth in response to boron toxicity. Plant Cell Environ 35:719–734

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Babula P, Adam V, Opatrilova R, Zehnalek J, Havel L, Kizek R (2008) Uncommon heavy metals, metalloids and their plant toxicity: a review. Environ Chem Lett 6:189–213

    Article  CAS  Google Scholar 

  • Bakhat HF, Zia Z, Fahad S, Abbas S, Hammad HM, Shahzad AN, Abbas F, Alharby H, Shahid M (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24:9142–9158

    Article  CAS  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  Google Scholar 

  • Benhamdi A, Bentellis A, Rached O, Du Laing G, Mechakra A (2014) Effects of antimony and arsenic on antioxidant enzyme activities of two steppic plant species in an old antimony mining area. Biol Trace Elem Res 158(1):96–104

    Article  CAS  Google Scholar 

  • Bhattacharjee H, Mukhopadhyay R, Thiyagarajan S, Rosen BP (2008) Aquaglyceroporins: ancient channels for metalloids. J Biol 7:33

    Article  CAS  Google Scholar 

  • Bienert GP, Tamás MJ (2018) Molecular mechanisms of metalloid transport, toxicity and tolerance. Front Cell Dev Biol 6:99

    Article  Google Scholar 

  • Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of as (OH)3 and Sb (OH)3 across membranes. BMC Biol 6:26

    Article  CAS  Google Scholar 

  • Bortey-Sam N, Nakayama SM, Ikenaka Y, Akoto O, Baidoo E, Yohannes YB, Mizukawa H, Ishizuka M (2015) Human health risks from metals and metalloid via consumption of food animals near gold mines in Tarkwa, Ghana: estimation of the daily intakes and target hazard quotients (THQs). Ecotoxicol Environ Saf 111:160–167

    Article  CAS  Google Scholar 

  • Brown TA, Shrift A (1980) Identification of selenocysteine in the proteins of selenate-grown Vigna radiata. Plant Physiol 66:758–761

    Article  CAS  Google Scholar 

  • Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Römheld V (2002) Boron in plant biology. Plant Biol 4:205–223

    Article  CAS  Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255

    Article  CAS  Google Scholar 

  • Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1; 1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133

    Article  CAS  Google Scholar 

  • Chakraborty M, Mukherjee A, Ahmed KM (2015) A review of groundwater arsenic in the Bengal Basin, Bangladesh and India: from source to sink. Curr Pollut Rep 1:220–247

    Article  CAS  Google Scholar 

  • Chang W, Chen TH, Pratt S, Shoback D (2000) Amino acids in the second and third intracellular loops of the parathyroid Ca2+-sensing receptor mediate efficient coupling to phospholipase C. J Biol Chem 275:19955–19963

    Article  CAS  Google Scholar 

  • Chen Y, Han YH, Cao Y, Zhu YG, Rathinasabapathi B, Ma LQ (2017) Arsenic transport in rice and biological solutions to reduce arsenic risk from rice. Front Plant Sci 8:268

    Google Scholar 

  • Cheong YH, Kim SU, Seo DC, Chang NI, Lee JB, Park JH et al (2009) Effect of inorganic and organic germanium treatments on the growth of lettuce (Lactuca sativa). J Korean Soc Appl Biol Chem 52(4):389–396

    Article  CAS  Google Scholar 

  • Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2014:1–12. https://doi.org/10.1155/2014/752708

    Article  CAS  Google Scholar 

  • Choi IW, Seo DC, Han MJ, DeLaune RD, Ok YS, Jeon WT et al (2013) Accumulation and toxicity of germanium in cucumber under different types of germaniums. Commun Soil Sci Plant Anal 44(20):3006–3019

    Article  CAS  Google Scholar 

  • Chung CC, Hwang SPL, Chang J (2003) Identification of a high-affinity phosphate transporter gene in a prasinophyte alga, Tetraselmis chui, and its expression under nutrient limitation. Appl Environ Microbiol 69:754–759

    Article  CAS  Google Scholar 

  • Cuypers A, Remans T, Weyens N, Colpaert J, Vassilev A, Vangronsveld J (2013) Soil–plant relationships of heavy metals and metalloids. In: Heavy metals in soils, Alloway BJ (Eds), Springer Netherlands, pp. 161–193

  • 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  Google Scholar 

  • De Schutter K, Joubès J, Cools T, Verkest A, Corellou F, Babiychuk E, Van Der Schueren E, Beeckman T, Kushnir S, Inze D, De Veylder L (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:211–225

    Article  CAS  Google Scholar 

  • Dimkovikj A, Van Hoewyk D (2014) Selenite activates the alternative oxidase pathway and alters primary metabolism in Brassica napus roots: evidence of a mitochondrial stress response. BMC Plant Biol 14:259

    Article  CAS  Google Scholar 

  • Ding X, Hua Y, Chen Y, Zhang C, Kong X (2015) Heavy metal complexation of thiol-containing peptides from soy glycinin hydrolysates. Int J Mol Sci 16(4):8040–8058

    Article  CAS  Google Scholar 

  • DiTusa SF, Fontenot EB, Wallace RW, Silvers MA, Steele TN, Elnagar AH, Dearman KM, Smith AP (2016) A member of the phosphate transporter 1 (Pht1) family from the arsenic-hyperaccumulating fern Pteris vittata is a high-affinity arsenate transporter. New Phytol 209:762–772

    Article  CAS  Google Scholar 

  • Durbak AR, Phillips KA, Pike S, O’Neill MA, Mares J, Gallavotti A, Malcomber ST, Gassmann W, McSteen P (2014) Transport of boron by the tassel-less1 aquaporin is critical for vegetative and reproductive development in maize. Plant Cell 26:2978–2995

    Article  CAS  Google Scholar 

  • El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241

    Article  CAS  Google Scholar 

  • El-Ramady H, Abdalla N, Alshaal T, El-Henawy A, Salah EDF, Shams MS, Shalaby T, Bayoumi Y, Elhawat N, Shehata S, Sztrik A (2015) Selenium and its role in higher plants. In: Pollutants in buildings, water and living organisms. Lichtfouse,E, Schwarzbauer J, Robert D (Eds), Springer Int Pub. Switzerland, pp. 235–296

  • Farooq MA, Islam F, Ali B, Najeeb U, Mao B, Gill RA, Yan G, Siddique KH, Zhou W (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52

    Article  CAS  Google Scholar 

  • Farrell N (2003) Metal complexes as drugs and chemotherapeutic agents. Compr Coord Chem II 9:809–840

  • Fasani E, Manara A, Martini F, Furini A, DalCorso G (2018) The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals. Plant Cell Environ 41:1201–1232

    Article  CAS  Google Scholar 

  • Favas PJC, Pratas J, Varun M, D’Souza R, Paul MS (2014) Phytoremediation of soils contaminated with metals and metalloids at mining areas: potential of native flora. In: Environmental risk assessment of soil contamination, Maria C. Hernandez-Soriano, IntechOpen, London, 3:485–516. https://doi.org/10.5772/57469

  • Feng R, Wei C, Tu S, Wu F, Yang L (2009) Antimony accumulation and antioxidative responses in four fern plants. Plant Soil 317:93–101

    Article  CAS  Google Scholar 

  • Feng R, Wei C, Tu S, Ding Y, Wang R, Guo J (2013) The uptake and detoxification of antimony by plants: a review. Environ Exp Bot 96:28–34

    Article  CAS  Google Scholar 

  • Filella M, Belzile N, Chen YW (2002) Antimony in the environment: a review focused on natural waters: I. Occurrence. Earth-Sci Rev 57:125–176

    Article  CAS  Google Scholar 

  • Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182

    Article  CAS  Google Scholar 

  • Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Van Hoewyk D, Pilon-Smits EA (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652

    Article  CAS  Google Scholar 

  • Fulekar MH, Anamika S, Bhaduri AM (2009) Genetic engineering strategies for enhancing phytoremediation of heavy metals. Afr J Biotechnol 8(4):529–535

    CAS  Google Scholar 

  • Gadd GM (1992) Metals and microorganisms: a problem of definition. FEMS Microbiol Lett 100(1–3):197–203

    Article  CAS  Google Scholar 

  • Garbinski LD, Rosen BP, Chen J (2019) Pathways of arsenic uptake and efflux. Environ Int 126:585–597

    Article  CAS  Google Scholar 

  • Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321

    Article  CAS  Google Scholar 

  • Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212

    Article  CAS  Google Scholar 

  • Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228

    Article  CAS  Google Scholar 

  • Grant K, Carey NM, Mendoza M, Schulze J, Pilon M, Pilon-Smits EA, Van Hoewyk D (2011) Adenosine 5′-phosphosulfate reductase (APR2) mutation in Arabidopsis implicates glutathione deficiency in selenate toxicity. Biochem J 438:325–335

    Article  CAS  Google Scholar 

  • Grün A, Buchner P, Broadley MR, Hawkesford MJ (2018) Identification and expression profiling of Pht1 phosphate transporters in wheat in controlled environments and in the field. Plant Biol 20:374–389

    Article  CAS  Google Scholar 

  • Gupta M, Gupta S (2017) An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci 7:2074

    Article  Google Scholar 

  • Gusman GS, Oliveira JA, Farnese FS, Cambraia J (2013) Arsenate and arsenite: the toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol Plant 35:1201–1209

    Article  CAS  Google Scholar 

  • Hasan M, 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

    Article  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Alhaithloul HAS, Parvin K, Bhuyan MHM, Tanveer M, Mohsin SM, Nahar K, Soliman MH, Mahmud JA, Fujita M (2019) Polyamine action under metal/metalloid stress: regulation of biosynthesis, metabolism, and molecular interactions. Int J Mol Sci 20:3215

    Article  CAS  Google Scholar 

  • Hassan Z, Aarts MG (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63

    Article  CAS  Google Scholar 

  • Hayes JE, Pallotta M, Baumann U, Berger B, Langridge P, Sutton T (2013) Germanium as a tool to dissect boron toxicity effects in barley and wheat. Funct Plant Biol 40:618–627

    Article  CAS  Google Scholar 

  • He M, Yang J (1999) Effects of different forms of antimony on rice during the period of germination and growth and antimony concentration in rice tissue. Sci Total Environ 243:149–155

    Article  Google Scholar 

  • Herath I, Vithanage M, Bundschuh J, Maity JP, Bhattacharya P (2016) Natural arsenic in global groundwaters: distribution and geochemical triggers for mobilization. Curr Pollut Rep 2:68–89

    Article  CAS  Google Scholar 

  • Hettick BE, Canas-Carrell JE, French AD, Klein DM (2015) Arsenic: a review of the element’s toxicity, plant interactions, and potential methods of remediation. J Agric Food Chem 63:7097–7107

    Article  CAS  Google Scholar 

  • 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. Aust J Bot:872875–872875

  • Hudek L, Premachandra D, Webster WAJ, Bräu L (2016) Role of phosphate transport system component PstB1 in phosphate internalization by Nostoc punctiforme. Appl Environ Microbiol 82:6344–6356

    Article  CAS  Google Scholar 

  • Hughes MF, Beck BD, Chen Y, Lewis AS, Thomas DJ (2011) Arsenic exposure and toxicology: a historical perspective. Toxicol Sci 123:305–332

    Article  CAS  Google Scholar 

  • Hugouvieux V, Dutilleul C, Jourdain A, Reynaud F, Lopez V, Bourguignon J (2009) Arabidopsis putative selenium-binding protein1 expression is tightly linked to cellular sulfur demand and can reduce sensitivity to stresses requiring glutathione for tolerance. Plant Physiol 151:768–781

    Article  CAS  Google Scholar 

  • Hummel RE (2011) Electrical properties of polymers, ceramics, dielectrics, and amorphous materials. In: Electronic properties of materials. Springer, New York, pp 181–211

    Chapter  Google Scholar 

  • Islam M, Karim M, Zheng X, Li X (2018) Heavy metal and metalloid pollution of soil, water and foods in Bangladesh: a critical review. Int J Environ Res Public Health 15:2825

    Article  CAS  Google Scholar 

  • Jahn TP, Bienert GP (2011) MIPs and Their Roles in the Exchange of Metalloids. Advances in Experimental Medicine and Biology, vol 679, Springer-Verlag, New York

  • Ji R, Zhou L, Liu J, Wang Y, Yang L, Zheng Q, Zhang C, Zhang B, Ge H, Yang Y, Zhao F (2017) Calcium-dependent protein kinase CPK31 interacts with arsenic transporter AtNIP1; 1 and regulates arsenite uptake in Arabidopsis thaliana. PLoS One 12:e0173681

    Article  CAS  Google Scholar 

  • Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 5:14

    Google Scholar 

  • Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    Article  CAS  Google Scholar 

  • Kmiecik E, Tomaszewska B, Wątor K, Bodzek M (2016) Selected problems with boron determination in water treatment processes. Part I: comparison of the reference methods for ICP-MS and ICP-OES determinations. Environ Sci Pollut Res 23:11658–11667

    Article  CAS  Google Scholar 

  • Kushwaha A, Rani R, Kumar S, Gautam A (2015) Heavy metal detoxification and tolerance mechanisms in plants: implications for phytoremediation. Environ Rev 24(1):39–51

    Article  CAS  Google Scholar 

  • Łabanowska M, Filek M, Kościelniak J, Kurdziel M, Kuliś E, Hartikainen H (2012) The effects of short-term selenium stress on Polish and Finnish wheat seedlings—EPR, enzymatic and fluorescence studies. J Plant Physiol 169:275–284

    Article  CAS  Google Scholar 

  • Lazard M, Dauplais M, Blanquet S, Plateau P (2017) Recent advances in the mechanism of selenoamino acids toxicity in eukaryotic cells. Biomol Concepts 8:93–104

    Article  CAS  Google Scholar 

  • Liao X, Zhang C, Sun G, Li Z, Shang L, Fu Y, He Y, Yang Y (2018) Assessment of metalloid and metal contamination in soils from Hainan, China. Int J Environ Res Public Health 15:454

    Article  CAS  Google Scholar 

  • Liu J, Yang L, Luan M, Wang Y, Zhang C, Zhang B, Shi J, Zhao FG, Lan W, Luan S (2015) A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc Natl Acad Sci U S A 112:E6571–E6578

    Article  CAS  Google Scholar 

  • Liu L, Li W, Song W, Guo M (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219

    Article  CAS  Google Scholar 

  • Lombi E, Holm PE (2010) Metalloids, soil chemistry and the environment. In: MIPs and their role in the exchange of metalloids. Springer, New York, pp 33–44

    Chapter  Google Scholar 

  • Lv Q, Wang L, Wang JZ, Li P, Chen YL, Du J, He YK, Bao F (2017) SHB1/HY1 alleviates excess boron stress by increasing BOR4 expression level and maintaining boron homeostasis in Arabidopsis roots. Front Plant Sci 8:790

    Article  Google Scholar 

  • Mahmood Q, Ahmad R, Kwak SS, Rashid A, Anjum NA (2010) Ascorbate and glutathione: protectors of plants in oxidative stress. In: Ascorbate-glutathione pathway and stress tolerance in plants, Anjum NA, Umar S, Chan M-T (Eds), Springer Netherlands, pp. 209–229. https://doi.org/10.1007/978-90-481-9404-9_7

  • Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H (2012) Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot 77:242–248

    Article  CAS  Google Scholar 

  • Mascher R, Lippmann B, Holzinger S, Bergmann H (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163:961–969

    Article  CAS  Google Scholar 

  • Masindi V, Muedi KL (2018) Environmental contamination by heavy metals. In: Heavy Metals, Hosam El-Din M. Saleh, Aglan R (Eds.) IntechOpen, Aglan, France, pp. 115–133

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  CAS  Google Scholar 

  • McCauley A, Jones C, Jacobsen J (2009) Plant nutrient functions and deficiency and toxicity symptoms. Nutrient management module, 9: 1–16. Mechanisms of plant defense response. Sci World J. https://doi.org/10.1155/2015/756120

  • Mirza N, Mahmood Q, Maroof Shah M, Pervez A, Sultan S (2014) Plants as useful vectors to reduce environmental toxic arsenic content. Sci World J. https://doi.org/10.1155/2014/921581

  • Molassiotis A, Sotiropoulos T, Tanou G, Diamantidis G, Therios I (2006) Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM 9 (Malus domestica Borkh). Environ Exp Bot 56:54–62

    Article  CAS  Google Scholar 

  • Mosa KA, Kumar K, Chhikara S, Mcdermott J, Liu Z, Musante C, White JC, Dhankher OP (2012) Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21:1265–1277

    Article  CAS  Google Scholar 

  • Mueckler M, Thorens B (2013) The SLC2 (GLUT) family of membrane transporters. Mol Asp Med 34:121–138

    Article  CAS  Google Scholar 

  • Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta 1840:1583–1591

    Article  CAS  Google Scholar 

  • Mustafa G, Komatsu S (2016) Toxicity of heavy metals and metal-containing nanoparticles on plants. Biochim Biophys Acta 1864:932–944

    Article  CAS  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  Google Scholar 

  • Navale AM, Paranjape AN (2016) Glucose transporters: physiological and pathological roles. Biophys Rev 8:5–9

    Article  CAS  Google Scholar 

  • Navazas A, Hendrix S, Cuypers A, González A (2019) Integrative response of arsenic uptake, speciation and detoxification by Salix atrocinerea. Sci Total Environ 689:422–433

    Article  CAS  Google Scholar 

  • Ngole-Jeme VM, Fantke P (2017) Ecological and human health risks associated with abandoned gold mine tailings contaminated soil. PLoS One 12:e0172517

    Article  CAS  Google Scholar 

  • Nielsen FH (2008) Essential and toxic trace elements in human health and disease. Curr Top Nutr Dis 18:277–292

    Google Scholar 

  • Nikolic D, Nesic S, Bosnic D, Kostic L, Nikolic M, Samardzic J (2019) Silicon alleviates iron deficiency in barley by enhancing expression of strategy II genes and metal redistribution. Front Plant Sci 10:416

    Article  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia BELEN, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35(2):454–484

    Article  CAS  Google Scholar 

  • Nussaume L, Kanno S, Javot H, Marin E, Nakanishi TM, Thibaud MC (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83

    Article  Google Scholar 

  • Ohkama-Ohtsu N, Zhao P, Xiang C, Oliver DJ (2007) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888

    Article  CAS  Google Scholar 

  • Ojuederie O, Babalola O (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14:1504

    Article  CAS  Google Scholar 

  • Ortega A, Garrido I, Casimiro I, Espinosa F (2017) Effects of antimony on redox activities and antioxidant defence systems in sunflower (Helianthus annuus L.) plants. PLoS One 12:e0183991

    Article  CAS  Google Scholar 

  • O'Shea B, Jankowski J, Sammut J (2007) The source of naturally occurring arsenic in a coastal sand aquifer of eastern Australia. Sci Total Environ 379:151–166

    Article  CAS  Google Scholar 

  • Pan X, Zhang D, Chen X, Bao A, Li L (2011) Antimony accumulation, growth performance, antioxidant defense system and photosynthesis of Zea mays in response to antimony pollution in soil. Water Air Soil Pollut 215(1–4):517–523

    Article  CAS  Google Scholar 

  • Phitsuwa P, Ratanakhanokchai K (2014) Can we create “elite rice”—a multifunctional crop for food, feed, and bioenergy production? Sustain Chem Process 2:10

    Article  CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574

    Article  CAS  Google Scholar 

  • Razzaq R (2017) Phytoremediation: an environmental friendly technique—a review. J Environ Anal Chem 4:2380–2391

    Article  Google Scholar 

  • Reardon AC (2011) Metallurgy for the non-metallurgist. 2nd Ed. ASM International, United States

  • Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ 27:1405–1414

    Article  CAS  Google Scholar 

  • Ren JH, Ma LQ, Sun HJ, Cai F, Luo J (2014) Antimony uptake, translocation and speciation in rice plants exposed to antimonite and antimonate. Sci Total Environ 475:83–89

    Article  CAS  Google Scholar 

  • Rengasamy P (2016) Soil chemistry factors confounding crop salinity tolerance—a review. Agronomy 6:53

    Article  CAS  Google Scholar 

  • Řezanka T, Sigler K (2008) Biologically active compounds of semi-metals. In: Studies in natural products chemistry, vol 35. Elsevier, pp 835–921. https://doi.org/10.1016/s1572-5995(08)80018-x

  • Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiol 142(3):1087–1101

    Article  CAS  Google Scholar 

  • Root RA, Hayes SM, Hammond CM, Maier RM, Chorover J (2015) Toxic metal (loid) speciation during weathering of iron sulfide mine tailings under semi-arid climate. Appl Geochem 62:131–149

    Article  CAS  Google Scholar 

  • Rottmann TM, Fritz C, Lauter A, Schneider S, Fischer C, Danzberger N, Sauer N, Stadler R (2018) Protoplast-esculin assay as a new method to assay plant sucrose transporters: characterization of AtSUC6 and AtSUC7 sucrose uptake activity in Arabidopsis Col-0 ecotype. Front Plant Sci 9:430

    Article  Google Scholar 

  • Salem HM, Abdel-Salam A, Abdel-Salam MA, Seleiman MF (2018) Phytoremediation of metal and metalloids from contaminated soil. In: Plants under metal and metalloid stress. Springer, Singapore, pp 249–262

    Chapter  Google Scholar 

  • Sankhla MS, Kumari M, Nandan M, Mohril S, Singh GP (2016) Effect of electronic waste on environmental and human health—a review. IOSR 10:98–104

    Article  CAS  Google Scholar 

  • Satapathy S, Panda CR (2018) Source identification, environmental risk assessment and human health risks associated with toxic elements present in a coastal industrial environment, India. Environ Geochem Health 40:2243–2257

    Article  CAS  Google Scholar 

  • Schiavon M, Moro I, Pilon-Smits EA, Matozzo V, Malagoli M, Dalla Vecchia F (2012) Accumulation of selenium in Ulva sp. and effects on morphology, ultrastructure and antioxidant enzymes and metabolites. Aquat Toxicol 122:222–231

    Article  CAS  Google Scholar 

  • Segawa H, Onitsuka A, Kuwahata M, Hanabusa E, Furutani J, Kaneko I, Tomoe Y, Aranami F, Matsumoto N, Ito M, Matsumoto M (2009) Type IIc sodium–dependent phosphate transporter regulates calcium metabolism. J Am Soc Nephrol 20:104–113

    Article  CAS  Google Scholar 

  • Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1-26. https://doi.org/10.1155/2012/217037

  • Sharma S, Singh B, Manchanda VK (2015) Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environ Sci Pollut Res 22:946–962

    Article  CAS  Google Scholar 

  • Sharma P, Srivastava V, Kumar A, Misra AN (2018) Mechanisms of metalloid uptake, transport, toxicity, and tolerance in plants. In: Emerging trends of plant physiology for sustainable crop production, Abbas Z, Tiwari AK, Kumar P (Eds), Apple Academic Press-CRC Press, United States, pp. 167–221

  • Shinmachi F, Buchner P, Stroud JL, Parmar S, Zhao FJ, McGrath SP, Hawkesford MJ (2010) Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium, and molybdenum in wheat. Plant Physiol 153:327–336

    Article  CAS  Google Scholar 

  • Shireen F, Nawaz M, Chen C, Zhang Q, Zheng Z, Sohail H, Sun J, Cao H, Huang Y, Bie Z (2018) Boron: functions and approaches to enhance its availability in plants for sustainable agriculture. Int J Mol Sci 19:1856

    Article  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72(4):1102–1110

    Article  CAS  Google Scholar 

  • Shtangeeva I, Bali R, Harris A (2011) Bioavailability and toxicity of antimony. J Geochem Explor 110(1):40–45

    Article  CAS  Google Scholar 

  • Shtangeeva I, Steinnes E, Lierhagen S (2012) Uptake of different forms of antimony by wheat and rye seedlings. Environ Sci Pollut Res 19:502–509

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kohli RK, Arora K (2007) Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53(1):65–73

    Article  CAS  Google Scholar 

  • Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharm 43:246–253

    Article  CAS  Google Scholar 

  • Singh VP, Singh S, Kumar J, Prasad SM (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  Google Scholar 

  • Smith KS, Huyck HL (1999) An overview of the abundance, relative mobility, bioavailability, and human toxicity of metals. Environ Geochem Miner Depos 6:29–70

    Google Scholar 

  • Smith FW, Rae AL, Hawkesford MJ (2000) Molecular mechanisms of phosphate and sulphate transport in plants. Biochim Biophys Acta 1465:236–245

    Article  CAS  Google Scholar 

  • Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant Soil 248:71–83

    Article  CAS  Google Scholar 

  • Soetan KO, Olaiya CO, Oyewole OE (2010) The importance of mineral elements for humans, domestic animals and plants—a review. Afr J Food Sci 4:200–222

    CAS  Google Scholar 

  • Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49(2):293–296

    Article  CAS  Google Scholar 

  • Su T, Li W, Wang P, Ma C (2019) Dynamics of peroxisome homeostasis and its role in stress response and signaling in plants. Front Plant Sci 10:705

    Article  Google Scholar 

  • Suman J, Uhlik O, Viktorova J, Macek T (2018) Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment? Front Plant Sci 9:1476

    Article  Google Scholar 

  • Tamás MJ, Wysocki R (2001) Mechanisms involved in metalloid transport and tolerance acquisition. Curr Genet 40:2–12

    Article  CAS  Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Molecular, clinical and environmental toxicology, Luch A (Eds), Springer, Basel, pp. 133–164

  • Terry N, Zayed AM, De Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Biol 51:401–432

    Article  CAS  Google Scholar 

  • Thorsen M, Di Y, Tängemo C, Morillas M, Ahmadpour D, Van der Does C, Wagner A, Johansson E, Boman J, Posas F, Wysocki R (2006) The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol Biol Cell 17:4400–4410

    Article  CAS  Google Scholar 

  • Turkez H (2008) Effects of boric acid and borax on titanium dioxide genotoxicity. J Appl Toxicol 28:658–664

    Article  CAS  Google Scholar 

  • Tytła M, Kostecki M (2019) Ecological risk assessment of metals and metalloid in bottom sediments of water reservoir located in the key anthropogenic “hot spot” area (Poland). Environ Earth Sci 78:179

    Article  CAS  Google Scholar 

  • Vaculík M, Mrázová A, Lux A (2015) Antimony (SbIII) reduces growth, declines photosynthesis, and modifies leaf tissue anatomy in sunflower (Helianthus annuus L.). Environ Sci Pollut Res 22:18699–18706

    Article  CAS  Google Scholar 

  • Van Hoewyk D (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann Bot 112:965–972

    Article  CAS  Google Scholar 

  • Vernon RE (2013) Which elements are metalloids? J Chem Educ 90:1703–1707

    Article  CAS  Google Scholar 

  • Wackett LP, Dodge AG, Ellis LB (2004) Microbial genomics and the periodic table. Appl Environ Microbiol 70:647–655

    Article  CAS  Google Scholar 

  • Wang X, Xu S, Zhou S, Xu W, Leary M, Choong P, Qian M, Brandt M, Xie YM (2016) Topological design and additive manufacturing of porous metals for bone scaffolds and orthopedic implants: a review. Biomaterials 83:127–141

    Article  CAS  Google Scholar 

  • Wang B, Li J, Gao J, Cai P, Han X, Tian C (2017a) Identification and characterization of the glucose dual-affinity transport system in Neurospora crassa: pleiotropic roles in nutrient transport, signaling, and carbon catabolite repression. Biotechnol Biofuels 10:17

    Article  CAS  Google Scholar 

  • Wang S, Yoshinari A, Shimada T, Hara-Nishimura I, Mitani-Ueno N, Ma JF, Naito S, Takano J (2017b) Polar localization of the NIP5; 1 boric acid channel is maintained by endocytosis and facilitates boron transport in Arabidopsis roots. Plant Cell 29:824–842

    Article  CAS  Google Scholar 

  • Weerakoon SR (2019) Genetic engineering for metal and metalloid detoxification. In: Transgenic plant technology for remediation of toxic metals and metalloids, Prasad MNV (Eds), Academic Press, United Kingdom, pp. 23–41

  • West G, Inzé D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058

    Article  CAS  Google Scholar 

  • White PJ (2015) Selenium accumulation by plants. Ann Bot 117:217–235

    Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  CAS  Google Scholar 

  • Wiche O, Székely B, Moschner C, Heilmeier H (2018) Germanium in the soil-plant system—a review. Environ Sci Pollut Res 25(32):31938–31956

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  CAS  Google Scholar 

  • Wilson NJ, Craw D, Hunter K (2004) Antimony distribution and environmental mobility at an historic antimony smelter site, New Zealand. Environ Pollut 129:257–266

    Article  CAS  Google Scholar 

  • Wisedchaisri G, Park MS, Iadanza MG, Zheng H, Gonen T (2014) Proton-coupled sugar transport in the prototypical major facilitator superfamily protein XylE. Nat Commun 5:4521

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology 2011:1–20. https://doi.org/10.5402/2011/402647

  • Zagorchev L, Seal C, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  CAS  Google Scholar 

  • Zangi R, Filella M (2012) Transport routes of metalloids into and out of the cell: a review of the current knowledge. Chem Biol Interact 197:47–57

    Article  CAS  Google Scholar 

  • Zhang Q, Chen H, He M, Zhao Z, Cai H, Ding G, Shi LXF (2017) The boron transporter BnaC4. BOR1; 1c is critical for inflorescence development and fertility under boron limitation in Brassica napus. Plant Cell Environ 40:1819–1833

    Article  CAS  Google Scholar 

  • Zhou X, Sun C, Zhu P, Liu F (2018) Effects of antimony stress on photosynthesis and growth of Acorus calamus. Front Plant Sci 9:579

    Article  Google Scholar 

  • Zwolak I, Zaporowska H (2012) Selenium interactions and toxicity: a review. Cell Biol Toxicol 28:31–46

    Article  CAS  Google Scholar 

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Author notes

  1. Simranjeet Singh, Vijay Kumar, Daljeet Singh Dhanjal and Dhriti Kapoor contributed equally to this work.

Authors and Affiliations

  1. Department of Biotechnology, Lovely Professional University, Phagwara, Punjab, 144411, India

    Simranjeet Singh, Daljeet Singh Dhanjal & Joginder Singh

  2. Punjab Biotechnology Incubator (PBTI), Phase-V, S.A.S. Nagar, Punjab, 160059, India

    Simranjeet Singh & Sanjay Kumar

  3. RAWTL, Department of Water Supply and Sanitation, Phase-II, S.A.S. Nagar, Punjab, 160054, India

    Simranjeet Singh, Satyender Singh & Sanjay Kumar

  4. Regional Ayurveda Research Institute for Drug Development, Gwalior, Madhya Pradesh, 474009, India

    Vijay Kumar

  5. Department of Zoology, Doaba College Jalandhar, Jalandhar, Punjab, 144001, India

    Shivika Datta

  6. Department of Botany, Lovely Professional University, Phagwara, Punjab, 144411, India

    Dhriti Kapoor

  7. Department of Botany, Mahatma Gandhi Central University, Motihari, Bihar, India

    Ram Prasad

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  1. Simranjeet Singh
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Singh, S., Kumar, V., Datta, S. et al. Physiological responses, tolerance, and remediation strategies in plants exposed to metalloids. Environ Sci Pollut Res 28, 40233–40248 (2021). https://doi.org/10.1007/s11356-020-10293-2

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