Skip to main content
SpringerLink
Log in

How metal hyperaccumulating plants can advance Zn biofortification

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background

Zn hyperaccumulating plants reach Zn concentrations in their leaves that are several hundredfold higher than the target values set for Zn-biofortified crops.

Scope

This extreme trait is relevant for Zn biofortification in various ways that are being discussed based on what is known about Zn hyperaccumulating plants.

Conclusions

First, Zn hyperaccumulation is the result of changes in metal homeostasis networks shared by all higher plants. It is not strictly dependent on high Zn levels in the soil. Thus, mechanistic insights gained from the study of Zn hyperaccumulators can support the breeding and engineering of Zn-biofortified crops. Second, certain plant families, the Brassicaceae in particular, appear to be genetically predispositioned to evolve enhanced Zn accumulation, suggesting the existence of intermediate species with elevated Zn concentrations in their leaves below the hyperaccumulation threshold or the potential to breed for such plants. This calls for extended screening especially among potential vegetable crops, ideally guided by knowledge about the at least partially convergent evolution of Zn hyperaccumulation. Third, the introduction of leafy vegetables with high Zn concentrations or even of Zn hyperaccumulator leaves into diets may represent a valid complementary biofortification approach.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Assuncao AGL, Bookum WM, Nelissen HJM, et al. (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  CAS  Google Scholar 

  • Assuncao AG, Pieper B, Vromans J, et al. (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 170:21–32

    Article  CAS  PubMed  Google Scholar 

  • Avato P, Argentieri MP (2015) Brassicaceae: a rich source of health improving phytochemicals. Phytochem Rev 14:1019–1033

    Article  CAS  Google Scholar 

  • Bashir K, Takahashi R, Nakanishi H, Nishizawa NK (2013) The road to micronutrient biofortification of rice: progress and prospects. Front Plant Sci 4:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268

    Article  CAS  PubMed  Google Scholar 

  • Bert V, Macnair MR, De Laguerie P, et al. (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol 146:225–234

    Article  CAS  Google Scholar 

  • Bert V, Bonnin I, Saumitou-Laprade P, et al. (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    Article  CAS  Google Scholar 

  • Björkman M, Klingen I, Birch ANE, et al. (2011) Phytochemicals of Brassicaceae in plant protection and human health - influences of climate, environment and agronomic practice. Phytochem 72:538–556

    Article  Google Scholar 

  • Blaauboer BJ, Boobis AR, Bradford B, et al. (2016) Considering new methodologies in strategies for safety assessment of foods and food ingredients. Food Chem Toxicol. doi:10.1016/j.fct.2016.02.019

    PubMed  Google Scholar 

  • Blair MW, Astudillo C, Rengifo J, et al. (2011) QTL analyses for seed iron and zinc concentrations in an intra-genepool population of Andean common beans (Phaseolus vulgaris L.). Theor Appl Genet 122:511–521

    Article  CAS  PubMed  Google Scholar 

  • Bouis HE, Welch RM (2010) Biofortification - a sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Sci 50:S20–S32

    Article  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, et al. (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20

    Article  CAS  Google Scholar 

  • Cappa JJ, Pilon-Smits EAH (2013) Evolutionary aspects of elemental hyperaccumulation. Planta 239:1–9

    Google Scholar 

  • Cavaiuolo M, Ferrante A (2014) Nitrates and glucosinolates as strong determinants of the nutritional quality in rocket leafy salads. Nutrients 6:1519–1538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens S (2014) Zn and Fe biofortification: the right chemical environment for human bioavailability. Plant Sci 225:52–57

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013a) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Deinlein U, Ahmadi H, et al. (2013b) Nicotianamine is a major player in plant Zn homeostasis. Biometals 26:623–632

    Article  CAS  PubMed  Google Scholar 

  • Cornu J-Y, Deinlein U, Höreth S, et al. (2015) Contrasting effects of nicotianamine synthase knockdown on zinc and nickel tolerance and accumulation in the zinc/cadmium hyperaccumulator Arabidopsis halleri. New Phytol 206:738–750

  • Courbot M, Willems G, Motte P, et al. (2007) A major QTL for Cd tolerance in Arabidopsis halleri co-localizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curie C, Cassin G, Couch D, et al. (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11

    Article  CAS  PubMed  Google Scholar 

  • Deinlein U, Weber M, Schmidt H, et al. (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24:708–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng T-H-B, Tang Y-T, van der EA, et al. (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil (in press). doi:10.1007/s11104-016-2825-1

    PubMed Central  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, et al. (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    Article  CAS  PubMed  Google Scholar 

  • Dräger DB, Desbrosses-Fonrouge AG, Krach C, et al. (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439

    Article  PubMed  Google Scholar 

  • EFSA (European Food Safety Authority) (2009) Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on cadmium in food. EFSA J 980:1–139

    Google Scholar 

  • Frérot H, Faucon M-P, Willems G, et al. (2010) Genetic architecture of zinc hyperaccumulation in Arabidopsis halleri: the essential role of QTL × environment interactions. New Phytol 187:355–367

  • Gao J, Sun L, Yang X, Liu J-X (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS One 8:e64643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genc Y, Verbyla AP, Torun AA, et al. (2009) Quantitative trait loci analysis of zinc efficiency and grain zinc concentration in wheat using whole genome average interval mapping. Plant Soil 314:49–66

    Article  CAS  Google Scholar 

  • Gibson RS (2012) Zinc deficiency and human health: etiology, health consequences, and future solutions. Plant Soil 361:291–299

    Article  CAS  Google Scholar 

  • Gowik U, Westhoff P (2011) The path from C-3 to C-4 photosynthesis. Plant Physiol 155:56–63

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Kim B, Kim S-H, Srivastava SK (2014) Molecular targets of isothiocyanates in cancer: recent advances. Mol Nutr Food Res 58:1685–1707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustin JL, Loureiro ME, Kim D, et al. (2009) MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J 57:1116–1127

    Article  CAS  PubMed  Google Scholar 

  • Halimaa P, Lin Y-F, Ahonen V, et al. (2014) Gene expression differences between Noccaea caerulescens ecotypes help identifying candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353

    Article  CAS  PubMed  Google Scholar 

  • Hambidge KM, Miller LV, Westcott JE, et al. (2010) Zinc bioavailability and homeostasis. Am J Clin Nutr 91:1478S–1483S

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond JP, Bowen HC, White PJ, et al. (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Kroymann J, Trampczynska A, et al. (2013) Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet 9:e1003707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howlett J, Edwards DG, Cockburn A, et al. (2003) The safety assessment of novel foods and concepts to determine their safety in use. Int J Food Sci Nutr 54:S1–S32

    Article  Google Scholar 

  • Kazemi-Dinan A, Thomaschky S, Stein RJ, et al. (2014) Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202:628–639

    Article  CAS  PubMed  Google Scholar 

  • Kozhevnikova AD, Seregin IV, Erlikh NT, et al. (2014) Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 203:508–519

    Article  CAS  PubMed  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Lee S, Persson DP, Hansen TH, et al. (2011) Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol J 9:865–873

    Article  CAS  PubMed  Google Scholar 

  • Lin Y-F, Hassan Z, Talukdar S, et al. (2016) Expression of the ZNT1 zinc transporter from the metal hyperaccumulator Noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana. PLoS One 11:e0149750

    Article  PubMed  PubMed Central  Google Scholar 

  • Lochlainn S, Bowen HC, Fray RG, et al (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS ONE 6:e17814. d

  • Lombi E, Zhao F, Dunham S, McGrath S (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20

    Article  CAS  Google Scholar 

  • Lonergan PF, Pallotta MA, Lorimer M, et al. (2009) Multiple genetic loci for zinc uptake and distribution in barley (Hordeum vulgare). New Phytol 184:168–179

    Article  CAS  PubMed  Google Scholar 

  • Mamo BE, Barber BL, Steffenson BJ (2014) Genome-wide association mapping of zinc and iron concentration in barley landraces from Ethiopia and Eritrea. J Cereal Sci 60:497–506

    Article  CAS  Google Scholar 

  • Maret W, Sandstead HH (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20:3–18

    Article  CAS  PubMed  Google Scholar 

  • Mills RF, Peaston KA, Runions J, Williams LE (2012) HvHMA2, a P1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS One 7:e42640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen LI, Palmgren MG (2014) Many rivers to cross: the journey of zinc from soil to seed. Front Plant Sci 5:30

    PubMed  PubMed Central  Google Scholar 

  • Olsen LI, Hansen TH, Larue C, et al. (2016) Mother-plant-mediated pumping of zinc into the developing seed. Nature Plants (in press). doi:10.1038/nplants.2016.36

    Google Scholar 

  • Pfeiffer WH, McClafferty B (2007) Harvestplus: breeding crops for better nutrition. Crop Sci 47:S88–S105

    Article  Google Scholar 

  • Phattarakul N, Rerkasem B, Li LJ, et al. (2012) Biofortification of rice grain with zinc through zinc fertilization in different countries. Plant Soil 361:131–141

    Article  CAS  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217-218:8–17

    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 

  • Ricachenevsky FK, Menguer PK, Sperotto RA, et al. (2013) Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front Plant Sci 4:144

    PubMed  PubMed Central  Google Scholar 

  • Ricachenevsky FK, Menguer PK, Sperotto RA, Fett JP (2015) Got to hide your Zn away: molecular control of Zn accumulation and biotechnological applications. Plant Sci 236:1–17

    Article  CAS  PubMed  Google Scholar 

  • Roohani N, Hurrell R, Kelishadi R, Schulin R (2013) Zinc and its importance for human health: an integrative review. J Res Med Sci 18:144–157

    PubMed  PubMed Central  Google Scholar 

  • Schuler M, Rellán-Álvarez R, Fink-Straube C, et al. (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24:2380–2400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott O, Galicia-Connolly E, Adams D, et al. (2012) The safety of cruciferous plants in humans: a systematic review. J Biomed Biotechnol 2012:503241

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahzad Z, Gosti F, Frerot H, et al. (2010) The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet 6:e1000911

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh SV, Singh K (2012) Cancer chemoprevention with dietary isothiocyanates mature for clinical translational research. Carcinogenesis 33:1833–1842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talke IN, Hanikenne M, Krämer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tauris B, Borg S, Gregersen PL, Holm PB (2009) A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J Exp Bot 60:1333–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomasi N, Pinton R, Dalla Costa L, et al. (2015) New “solutions” for floating cultivation system of ready-to-eat salad: a review. Trends Food Sci Technol 46:267–276

    Article  CAS  Google Scholar 

  • van de Mortel JE, Almar Villanueva L, Schat H, et al. (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, et al. (2012) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  CAS  PubMed  Google Scholar 

  • Verbruggen N, Hanikenne M, Clemens S (2013) A more complete picture of metal hyperaccumulation through next-generation sequencing technologies. Front Plant Sci 4:388

    Article  PubMed  PubMed Central  Google Scholar 

  • Warwick SI (2011) Brassicaceae in Agriculture. In: R. Schmidt, I. Bancroft (eds.), Genetics and Genomics of the Brassicaceae, Plant Genetics and Genomics: Crops and Models 9, Springer.

  • Weber M, Harada E, Vess C, et al. (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets - iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Broadley MR (2011) Physiological limits to zinc biofortification of edible crops. Front Plant Sci 2:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Willems G, Dräger DB, Courbot M, et al. (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willems G, Frerot H, Gennen J, et al. (2010) Quantitative trait loci analysis of mineral element concentrations in an Arabidopsis halleri x Arabidopsis lyrata petraea F2 progeny grown on cadmium-contaminated soil. New Phytol 187:368–379

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I am grateful to Mark Aarts for discussions and to Hassan Ahmadi for the A. halleri picture. Work in the author’s laboratory on Zn hyperaccumulation is supported by the Deutsche Forschungsgemeinschaft (CL 152/9-2).

Author information

Authors and Affiliations

  1. Department of Plant Physiology, University of Bayreuth, Universitätsstrasse 30, 95440, Bayreuth, Germany

    Stephan Clemens

Authors
  1. Stephan Clemens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephan Clemens.

Additional information

Responsible Editor: Philip John White.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Clemens, S. How metal hyperaccumulating plants can advance Zn biofortification. Plant Soil 411, 111–120 (2017). https://doi.org/10.1007/s11104-016-2920-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-2920-3

Keywords

Search

Navigation