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Current Advances in Fern Research pp 361–379Cite as

Novel Genes of Hyperaccumulator Ferns in Arsenic Tolerance, Uptake, and Metabolism: Implications for Crop Improvement

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Abstract

Fern evolution represents plant adaptations to abiotic stress conditions such as metal-contaminated soils and calcareous soils. Although these adaptations are known for a long time, few attempts have been made to understand the genetic and physiological mechanisms behind such tolerance to environmental stress. It was proposed that the genes controlling these traits could be novel sources to improve plants due to the availability of transgenic technologies. Among ferns in Pteridales, the taxa with the largest number of species diversity, certain ferns have evolved an extraordinary capacity to accumulate the toxic metalloid arsenic. This trait, both for its biological curiosity and potential utility for phytoremediation and crop improvement, has made the arsenic-hyperaccumulator Pteris vittata (Chinese brake fern) at the center of research studies for the past two decades. Genes related to arsenic uptake, transport, and translocation, redox homeostasis, and arsenic metabolism have been identified. The objective of this review is to summarize research in this area with a specific purpose to point out how the fern genes could be utilized to engineer plants with little ability to take up and accumulate arsenic for arsenic phytoremediation and to engineer crop plants to have improved tolerance to abiotic stress, thus potentially improving soil remediation and food security.

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References

  • Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128(3):1120–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali W, Isayenkov SV, Zhao FJ, Maathuis FJM (2009) Arsenite transport in plants. Cell Mol Life Sci 66(14):2329–2339

    Article  CAS  PubMed  Google Scholar 

  • Ali W, Isner JC, Isayenkov SV, Liu W, Zhao FJ, Maathuis FJM (2012) Heterologous expression of the yeast arsenite efflux system ACR3 improves Arabidopsis thaliana tolerance to arsenic stress. New Phytol 194(3):716–723

    Article  CAS  PubMed  Google Scholar 

  • Argos M, Kalra T, Rathouz PJ, Chen Y, Pierce B, Parvez F, Islam T, Ahmed A, Rakibuz-Zaman M, Hasan R, Sarwar G, Slavkovich V, van Geen A, Graziano J, Ahsan H (2010) Arsenic exposure from drinking water, and all-cause and chronic-disease mortalities in Bangladesh (HEALS): a prospective cohort study. Lancet 376(9737):252–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bech J, Poschenrieder C, Llugany M, Barcelo J, Tume P, Tobias FJ, Barranzuela JL, Vasquez ER (1997) Arsenic and heavy metal contamination of soil and vegetation around a copper mine in Northern Peru. Sci Total Environ 203(1):83–91

    Article  CAS  Google Scholar 

  • Bhattacharjee H, Rosen BP (2007) Arsenic metabolism in prokaryotic and eukaryotic microbes. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals. Springer, Berlin/Heidelberg, pp 371–406

    Chapter  Google Scholar 

  • Bienert GP, Thorsen M, Schussler MD, Nilsson HR, Wagner A, Tamas 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  PubMed  PubMed Central  CAS  Google Scholar 

  • Bobrowicz P, Wysocki R, Owsianik G, Goffeau A, Ulaszewski S (1997) Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 13(9):819–828

    Article  CAS  PubMed  Google Scholar 

  • Bondada BR, Tu S, Ma LQ (2004) Absorption of foliar-applied arsenic by the arsenic hyperaccumulating fern (Pteris vittata L.) Sci Total Environ 332(1):61–70

    Article  CAS  PubMed  Google Scholar 

  • Brinch-Pedersen H, Sorensen LD, Holm PB (2002) Engineering crop plants: getting a handle on phosphate. Trends Plant Sci 7(3):118–125

    Article  CAS  PubMed  Google Scholar 

  • Caille N, Zhao FJ, McGrath SP (2005) Comparison of root absorption, translocation and tolerance of arsenic in the hyperaccumulator Pteris vittata and the nonhyperaccumulator Pteris tremula. New Phytol 165(3):755–761

    Article  CAS  PubMed  Google Scholar 

  • Cantamessa S, D'Agostino G, Berta G (2016) Hydathode structure and localization in Pteris vittata fronds and evidence for their involvement in arsenic leaching. Plant Biosys Int J Dealing Asp Plant Biol 150(6):1208–1215

    Google Scholar 

  • Cesaro P, Cattaneo C, Bona E, Berta G, Cavaletto M (2015) The arsenic hyperaccumulating Pteris vittata expresses two arsenate reductases. Sci Rep 5:14525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, Zhao FJ, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12(12):e1002009

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125(3):1206–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Xu W, Shen H, Yan H, He Z, Ma M (2013) Engineering arsenic tolerance and hyperaccumulation in plants for phytoremediation by a PvACR3 transgenic approach. Environ Sci Technol 47(16):9355–9362

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Fu J-W, Han Y-H, Rathinasabapathi B, Ma LQ (2016) High as exposure induced substantial arsenite efflux in As-hyperaccumulator Pteris vittata. Chemosphere 144:2189–2194

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Chen Y, Hua CY, Jia MR, Fu JW, Liu X, Han YH, Liu Y, Rathinasabapathi B, Cao Y, Ma LQ (2017b) Heterologous expression of Pteris vittata arsenite antiporter PvACR3;1 reduces arsenic accumulation in plant shoots. Environ Sci Technol 51(18):10387–10395

    Article  CAS  PubMed  Google Scholar 

  • Clark GT, Dunlop J, Phung HT (2000) Phosphate absorption by Arabidopsis thaliana: interactions between phosphorus status and inhibition by arsenate. Aust J Plant Physiol 27(10):959–965

    CAS  Google Scholar 

  • Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18(12):3325–3333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123(3):825–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19(2):292–305

    Article  Google Scholar 

  • Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Datta R, Das P, Tappero R, Punamiya P, Elzinga E, Sahi S, Feng H, Kiiskila J, Sarkar D (2017) Evidence for exocellular arsenic in fronds of Pteris vittata. Sci Rep 7(1):2839

    Article  PubMed  PubMed Central  Google Scholar 

  • Dekoe T (1994) Agrostis castellana and Agrostis delicatula on heavy metal and arsenic enriched sites in NE Portugal. Sci Total Environ 145(1–2):103–109

    Article  CAS  Google Scholar 

  • Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2). Proc Natl Acad Sci U S A 103(14):5413–5418

    Article  CAS  PubMed  PubMed Central  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(2):762–772

    Article  CAS  PubMed  Google Scholar 

  • Dong RB, Formentin E, Losseso C, Carimi F, Benedetti P, Terzi M, Lo Schiavo F (2005) Molecular cloning and characterization of a phytochelatin synthase gene, PvPCS1, from Pteris vittata L. J Ind Microbiol Biotechnol 32(11–12):527–533

    Article  CAS  PubMed  Google Scholar 

  • Duan GL, Zhu YG, Tong YP, Cai C, Kneer R (2005) Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiol 138(1):461–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan G-L, Zhou Y, Tong Y-P, Mukhopadhyay R, Rosen BP, Zhu Y-G (2007) A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174(2):311–321

    Article  CAS  PubMed  Google Scholar 

  • Duan GL, Kamiya T, Ishikawa S, Arao T, Fujiwara T (2012) Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell Physiol 53(1):154–163

    Article  CAS  PubMed  Google Scholar 

  • Ellis DR, Gumaelius L, Indriolo E, Pickering IJ, Banks JA, Salt DE (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 141(4):1544–1554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  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 

  • Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9(3):303–321

    Article  CAS  Google Scholar 

  • Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 96(9):5001–5006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert N (2009) Environment: the disappearing nutrient. Nature 461(7265):716–718

    Article  CAS  PubMed  Google Scholar 

  • Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86(18):6838–6842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gumaelius L, Lahner B, Salt DE, Banks JA (2004) Arsenic hyperaccumulation in gametophytes of Pteris vittata. A new model system for analysis of arsenic hyperaccumulation. Plant Physiol 136(2):3198–3208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo JB, Dai XJ, Xu WZ, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72(7):1020–1026

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Bhatnagar AK (2015) Spatial distribution of arsenic in different leaf tissues and its effect on structure and development of stomata and trichomes in mung bean, Vigna radiata (L.) Wilczek. Environ Exp Bot 109:12–22

    Article  CAS  Google Scholar 

  • Han YH, Yang GM, Fu JW, Guan DX, Chen Y, Ma LQ (2016) Arsenic-induced plant growth of arsenic-hyperaccumulator Pteris vittata: impact of arsenic and phosphate rock. Chemosphere 149:366–372

    Article  CAS  PubMed  Google Scholar 

  • Han Y-H, Liu X, Rathinasabapathi B, Li H-B, Chen Y, Ma LQ (2017a) Mechanisms of efficient as solubilization in soils and as accumulation by As-hyperaccumulator Pteris vittata. Environ Pollut 227:569–577

    Article  CAS  PubMed  Google Scholar 

  • Han YH, Fu JW, Xiang P, Cao Y, Rathinasabapathi B, Chen Y, Ma LQ (2017b) Arsenic and phosphate rock impacted the abundance and diversity of bacterial arsenic oxidase and reductase genes in rhizosphere of As-hyperaccumulator Pteris vittata. J Hazard Mater 321:146–153

    Article  CAS  PubMed  Google Scholar 

  • Handson PD (1984) Lead and arsenic levels in wines produced from vineyards where lead arsenate sprays are used for caterpillar control. J Sci Food Agric 35(2):215–218

    Article  CAS  PubMed  Google Scholar 

  • Hayashi S, Kuramata M, Abe T, Takagi H, Ozawa K, Ishikawa S (2017) Phytochelatin synthase OsPCS1 plays a crucial role in reducing arsenic levels in rice grains. Plant J 91(5):840–848

    Article  CAS  PubMed  Google Scholar 

  • He Z, Yan H, Chen Y, Shen H, Xu W, Zhang H, Shi L, Zhu YG, Ma M (2016) An aquaporin PvTIP4;1 from Pteris vittata may mediate arsenite uptake. New Phytol 209(2):746–761

    Article  CAS  PubMed  Google Scholar 

  • Heiss S, Wachter A, Bogs J, Cobbett C, Rausch T (2003) Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure. J Exp Bot 54(389):1833–1839

    Article  CAS  PubMed  Google Scholar 

  • Hirano S (2004) The accumulation and toxicity of methylated arsenicals in endothelial cells: important roles of thiol compounds. Toxicol Appl Pharmacol 198(3):458–467

    Article  CAS  PubMed  Google Scholar 

  • Huang JW, Poynton CY, Kochian LV, Elless MP (2004) Phytofiltration of arsenic from drinking water using arsenic-hyperaccumulating ferns. Environ Sci Technol 38(12):3412–3417

    Article  CAS  PubMed  Google Scholar 

  • Huang J-H, Hu K-N, Decker B (2011) Organic arsenic in the soil environment: speciation, occurrence, transformation, and adsorption behavior. Water Air Soil Pollut 219(1–4):401–415

    Article  CAS  Google Scholar 

  • Indriolo E, Na G, Ellis D, Salt DE, Banks JA (2010) A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22(6):2045–2057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isayenkov SV, Maathuis FJ (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582(11):1625–1628

    Article  CAS  PubMed  Google Scholar 

  • Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    Article  PubMed  Google Scholar 

  • Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol 156(3):1164–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M (2011) Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 31(2):95–107

    CAS  PubMed  Google Scholar 

  • Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284(4):2114–2120

    Article  CAS  PubMed  Google Scholar 

  • Kertulis GM, Ma LQ, MacDonald GE, Chen R, Winefordner JD, Cai Y (2005) Arsenic speciation and transport in Pteris vittata L. and the effects on phosphorus in the xylem sap. Environ Exp Bot 54(3):239–247

    Article  CAS  Google Scholar 

  • Kramer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16(2):133–141

    Article  PubMed  CAS  Google Scholar 

  • Kupper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212(1):75–84

    Article  CAS  PubMed  Google Scholar 

  • Landrieu I, Hassan S, Sauty M, Dewitte F, Wieruszeski J-M, Inzé D, Veylder LD, Lippens G (2004) Characterization of the Arabidopsis thaliana Arath; CDC25 dual-specificity tyrosine phosphatase. Biochem Biophys Res Commun 322(3):734–739

    Article  CAS  PubMed  Google Scholar 

  • Lepp NW (1975) Potential of tree-ring analysis for monitoring heavy-metal pollution patterns. Environ Pollut 9(1):49–61

    Article  CAS  Google Scholar 

  • Lessl JT, Ma LQ (2013) Sparingly-soluble phosphate rock induced significant plant growth and arsenic uptake by Pteris vittata from three contaminated soils. Environ Sci Technol 47(10):5311–5318

    Article  CAS  PubMed  Google Scholar 

  • Lessl JT, Ma LQ, Rathinasabapathi B, Guy C (2013) Novel phytase from Pteris vittata resistant to arsenate, high temperature, and soil deactivation. Environ Sci Technol 47(5):2204–2211

    Article  CAS  PubMed  Google Scholar 

  • Li WX, Chen TB, Chen Y, Lei M (2005) Role of trichome of Pteris vittata L. in arsenic hyperaccumulation. Sci China C Life Sci 48(2):148–154

    Article  CAS  PubMed  Google Scholar 

  • Liu WJ, Wood BA, Raab A, McGrath SP, Zhao FJ, Feldmann J (2010) Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. Plant Physiol 152(4):2211–2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Schat H, Bliek M, Chen Y, McGrath SP, George G, Salt DE, Zhao FJ (2012) Knocking out ACR2 does not affect arsenic redox status in Arabidopsis thaliana: implications for as detoxification and accumulation in plants. PLoS One 7(8):e42408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156(2):195–203

    Article  CAS  Google Scholar 

  • Ma LQ, Komar KM, Tu C, Zhang WH, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic - a hardy, versatile, fast-growing plant helps to remove arsenic from contaminated soils. Nature 409(6820):579–579

    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. Proc Natl Acad Sci U S A 105(29):9931–9935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathews S, Rathinasabapathi B, Ma LQ (2011) Uptake and translocation of arsenite by Pteris vittata L.: effects of glycerol, antimonite and silver. Environ Pollut 159(12):3490–3495

    Article  CAS  PubMed  Google Scholar 

  • Matschullat J (2000) Arsenic in the geosphere - a review. Sci Total Environ 249(1–3):297–312

    Article  CAS  PubMed  Google Scholar 

  • Meharg AA (2003) Variation in arsenic accumulation - hyperaccumulation in ferns and their allies. New Phytol 157(1):25–31

    Article  CAS  Google Scholar 

  • Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154(1):29–43

    Article  CAS  Google Scholar 

  • Meharg AA, Macnair MR (1992) Suppression of the high-affinity phosphate-uptake system - a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43(249):519–524

    Article  CAS  Google Scholar 

  • Meharg AA, Naylor J, Macnair MR (1994) Phosphorus nutrition of arsenate-tolerant and nontolerant phenotypes of velvetgrass. J Environ Qual 23(2):234–238

    Article  CAS  Google Scholar 

  • Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62(12):4391–4398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Jimenez E, Esteban E, Penalosa JM (2012) The fate of arsenic in soil-plant systems. Rev Environ Contam Toxicol 215:1–37

    PubMed  Google Scholar 

  • Moreno-Jimenez E, Six L, Williams PN, Smolders E (2013) Inorganic species of arsenic in soil solution determined by microcartridges and ferrihydrite-based diffusive gradient in thin films (DGT). Talanta 104:83–89

    Article  CAS  PubMed  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(6):1265–1277

    Article  CAS  PubMed  Google Scholar 

  • Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci U S A 93(19):10519–10523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay R, Rosen BP (1998) Saccharomyces cerevisiae ACR2 gene encodes an arsenate reductase. FEMS Microbiol Lett 168(1):127–136

    Article  CAS  PubMed  Google Scholar 

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300(5621):939–944

    Article  CAS  PubMed  Google Scholar 

  • Pal R, Rai JP (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160(3):945–963

    Article  CAS  PubMed  Google Scholar 

  • Pandey N, Gupta B, Pathak GC (2013) Foliar application of Zn at flowering stage improves plant's performance, yield and yield attributes of black gram. Indian J Exp Biol 51(7):548–555

    CAS  PubMed  Google Scholar 

  • Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks JA, Salt DE, George GN (2006) Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol 40(16):5010–5014

    Article  CAS  PubMed  Google Scholar 

  • Poynton CY, Huang JWW, Blaylock MJ, Kochian LV, Elless MP (2004) Mechanisms of arsenic hyperaccumulation in Pteris species: root as influx and translocation. Planta 219(6):1080–1088

    Article  CAS  PubMed  Google Scholar 

  • Puckett EE, Serapiglia MJ, DeLeon AM, Long S, Minocha R, Smart LB (2012) Differential expression of genes encoding phosphate transporters contributes to arsenic tolerance and accumulation in shrub willow (Salix spp.) Environ Exp Bot 75:248–257

    Article  CAS  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3(1):1–17

    Google Scholar 

  • Rathinasabapathi B (2006) Ferns represent an untapped biodiversity for improving crops for environmental stress tolerance. New Phytol 172(3):385–390

    Article  PubMed  Google Scholar 

  • Rathinasabapathi B, Wu S, Sundaram S, Rivoal J, Srivastava M, Ma LQ (2006) Arsenic resistance in Pteris vittata L.: identification of a cytosolic triosephosphate isomerase based on cDNA expression cloning in Escherichia coli. Plant Mol Biol 62(6):845–857

    Article  CAS  PubMed  Google Scholar 

  • Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci 60(2):124–143

    Article  CAS  Google Scholar 

  • Ronzan M, Zanella L, Fattorini L, Della Rovere F, Urgast D, Cantamessa S, Nigro A, Barbieri M, Sanità di Toppi L, Berta G, Feldmann J, Altamura MM, Falasca G (2017) The morphogenic responses and phytochelatin complexes induced by arsenic in Pteris vittata change in the presence of cadmium. Environ Exp Bot 133:176–187

    Article  CAS  Google Scholar 

  • Rosen BP (1999) Families of arsenic transporters. Trends Microbiol 7(5):207–212

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Bermejo E, Castrillo G, del Llano B, Navarro C, Zarco-Fernández S, Martinez-Herrera DJ, Leo-del Puerto Y, Muñoz R, Cámara C, Paz-Ares J, Alonso-Blanco C, Leyva A (2014) Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat Commun 5:4617

    Article  PubMed  CAS  Google Scholar 

  • Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53(379):2381–2392

    Article  CAS  PubMed  Google Scholar 

  • Schmoger ME, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122(3):793–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen S, Li X-F, Cullen WR, Weinfeld M, Le XC (2013) Arsenic binding to proteins. Chem Rev 113(10):7769–7792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi GL, Zhu S, Meng JR, Qian M, Yang N, Lou LQ, Cai QS (2015) Variation in arsenic accumulation and translocation among wheat cultivars: the relationship between arsenic accumulation, efflux by wheat roots and arsenate tolerance of wheat seedlings. J Hazard Mater 17:190–196

    Article  CAS  Google Scholar 

  • Shi S, Wang T, Chen Z, Tang Z, Wu Z, Salt DE, Chao D-Y, Zhao F-J (2016) OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol 172(3):1708–1719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shri M, Dave R, Diwedi S, Shukla D, Kesari R, Tripathi RD, Trivedi PK, Chakrabarty D (2014) Heterologous expression of Ceratophyllum demersum phytochelatin synthase, CdPCS1, in rice leads to lower arsenic accumulation in grain. Sci Rep 4(1):5784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sneller FE, van Heerwaarden LM, Koevoets PL, Vooijs R, Schat H, Verkleij JA (2000) Derivatization of phytochelatins from Silene vulgaris, induced upon exposure to arsenate and cadmium: comparison of derivatization with Ellman’s reagent and monobromobimane. J Agric Food Chem 48(9):4014–4019

    Article  CAS  PubMed  Google Scholar 

  • Sohn E (2014) Contamination: the toxic side of rice. Nature 514(7524):S62–S63

    Article  PubMed  Google Scholar 

  • Srivastava M, Ma LQ, Santos JAG (2006) Three new arsenic hyperaccumulating ferns. Sci Total Environ 364(1–3):24–31

    Article  CAS  PubMed  Google Scholar 

  • Srivastava M, Santos J, Srivastava P, Ma LQ (2010) Comparison of arsenic accumulation in 18 fern species and four Pteris vittata accessions. Bioresour Technol 101(8):2691–2699

    Article  CAS  PubMed  Google Scholar 

  • Stone R (2008) Arsenic and paddy rice: a neglected cancer risk? Science 321(5886):184–185

    Article  CAS  PubMed  Google Scholar 

  • Su YH, McGrath SP, Zhu YG, Zhao FJ (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 180(2):434–441

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Rathinasabapathi B (2010) Transgenic expression of fern Pteris vittata glutaredoxin PvGrx5 in Arabidopsis thaliana increases plant tolerance to high temperature stress and reduces oxidative damage to proteins. Planta 231(2):361–369

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283(10):6095–6101

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Wu S, Ma LQ, Rathinasabapathi B (2009) Expression of a Pteris vittata glutaredoxin PvGRX5 in transgenic Arabidopsis thaliana increases plant arsenic tolerance and decreases arsenic accumulation in the leaves. Plant Cell Environ 32(7):851–858

    Article  CAS  PubMed  Google Scholar 

  • Tu C, Ma LQ, Bondada B (2002) Arsenic accumulation in the hyperaccumulator Chinese brake and its utilization potential for phytoremediation. J Environ Qual 31(5):1671–1675

    Article  CAS  PubMed  Google Scholar 

  • Tu C, Ma LQ, Zhang W, Cai Y, Harris WG (2003) Arsenic species and leachability in the fronds of the hyperaccumulator Chinese brake (Pteris vittata L.) Environ Pollut 124(2):223–230

    Article  CAS  PubMed  Google Scholar 

  • Turner BL, Paphazy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos Trans R Soc Lond Ser B Biol Sci 357(1420):449–469

    Article  CAS  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci U S A 96(12):7110–7115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visoottiviseth P, Francesconi K, Sridokchan W (2002) The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut 118(3):453–461

    Article  CAS  PubMed  Google Scholar 

  • Wang JR, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130(3):1552–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang HB, Ye ZH, Shu WS, Li WC, Wong MH, Lan CY (2006) Arsenic uptake and accumulation in fern species growing at arsenic-contaminated sites of southern China: field surveys. Int J Phytoremediation 8(1):1–11

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhang W, Mao C, Xu G, Zhao F-J (2016) The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. J Exp Bot 67(21):6051–6059

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Na G, Bermejo ES, Chen Y, Banks JA, Salt DE, Zhao FJ (2017) Dissecting the components controlling root-to-shoot arsenic translocation in Arabidopsis thaliana. New Phytol 31(10):14761

    Google Scholar 

  • Wysocki R, Bobrowicz P, Ulaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem 272(48):30061–30066

    Article  CAS  PubMed  Google Scholar 

  • Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176(3):590–599

    Article  CAS  PubMed  Google Scholar 

  • Xu JY, Li HB, Liang S, Luo J, Ma LQ (2014) Arsenic enhanced plant growth and altered rhizosphere characteristics of hyperaccumulator Pteris vittata. Environ Pollut 194:105–111

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Dai W, Yan H, Li S, Shen H, Chen Y, Xu H, Sun Y, He Z, Ma M (2015) Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8(5):722–733

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Shi S, Wang L, Tang Z, Lv T, Zhu X, Ding X, Wang Y, Zhao F-J, Wu Z (2017) OsHAC4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytol 215(3):1090–1101

    Article  CAS  PubMed  Google Scholar 

  • Yan X-L, Liao X-Y, T-b C (2009) Leaching potential of arsenic from Pteris vittata L. under field conditions. Sci Total Environ 408(2):425–430

    Article  CAS  PubMed  Google Scholar 

  • Yang M (2011) A current global view of environmental and occupational cancers. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 29(3):223–249

    Article  CAS  PubMed  Google Scholar 

  • Yang XX, Chen H, Dai XJ, Xu WZ, He ZY, Ma M (2009) Evidence of vacuolar compartmentalization of arsenic in the hyperaccumulator Pteris vittata. Chin Sci Bull 54(22):4229–4233

    Article  CAS  Google Scholar 

  • Zhang WH, Cai Y, Tu C, Ma LQ (2002) Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci Total Environ 300(1–3):167–177

    CAS  PubMed  Google Scholar 

  • Zhao FJ, Dunham SJ, McGrath SP (2002) Arsenic hyperaccumulation by different fern species. New Phytol 156(1):27–31

    Article  CAS  Google Scholar 

  • Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol 159(2):403–410

    Article  CAS  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181(4):777–794

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186(2):392–399

    Article  CAS  PubMed  Google Scholar 

  • Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42:443–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 21707068 and 21637002), Jiangsu Provincial Natural Science Foundation of China (Grant No. BK20160649), and the National Key Research and Development Program of China (Grant No. 2016YFD0800801).

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Authors and Affiliations

  1. State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Jiangsu, China

    Yanshan Chen, Yue Cao & Lena Ma

  2. Horticultural Sciences Department, University of Florida, Gainesville, FL, USA

    Bala Rathinasabapathi

  3. Soil and Water Science Department, University of Florida, Gainesville, FL, USA

    Lena Ma

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  1. Yanshan Chen
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  2. Yue Cao
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  3. Bala Rathinasabapathi
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  4. Lena Ma
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Correspondence to Yanshan Chen .

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  1. Department of Organisms and Systems Biology, Oviedo University, Oviedo, Spain

    Helena Fernández

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Chen, Y., Cao, Y., Rathinasabapathi, B., Ma, L. (2018). Novel Genes of Hyperaccumulator Ferns in Arsenic Tolerance, Uptake, and Metabolism: Implications for Crop Improvement. In: Fernández, H. (eds) Current Advances in Fern Research. Springer, Cham. https://doi.org/10.1007/978-3-319-75103-0_17

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