Skip to main content
Log in

Plant growth regulators-assisted phytoextraction

  • Review
  • Published:
Biologia Plantarum

Abstract

Plant growth regulators (PRG)-assisted phytoremediation is a technique that could enhance the yield of heavy metal accumulation in plant tissues. So far, a small number of experiments have helped identify three groups of plant hormones that may be useful for this purpose: auxins, cytokinins, and gibberellins. Studies have shown that these hormones positively affect the degree of accumulation of metallic impurities and improve the growth and stress resistance of plants. This review summarizes the present knowledge about PGRs’ impact on phytoextraction yield.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

BAP:

6-benzylaminopurine

EDDS:

ethylenediamine-N,N′-disuccinic acid

EDTA:

ethylenediaminetetraacetic acid

GA3 :

gibberellic acid

IAA:

indole-3-acetic acid

IBA:

indole-3-butyric acid

JA:

jasmonic acid

NAA:

naphthylacetic acid

NLMMOA:

natural low molecular mass organic acids

NTA:

nitrilotriacetic acid

PAA:

phenylacetic acid

PGR:

plant growth regulators

References

  • Appenroth, K.J.: Definition of “heavy metals” and their role in biological systems. — In: Sherameti, I., Varma, A. (ed.): Soil Heavy Metals. Pp. 19–29. Springer, Berlin — Heidelberg 2010.

    Chapter  Google Scholar 

  • Bajguz, A., Hayat, S.: Effects of brassinosteroids on the plant responses to environmental stresses. — Plant Physiol. Biochem. 47: 1–8, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Baker, A.J.M.: Zinc-phosphorus interaction in a zinc-tolerant and a non-tolerant population of Silene maritima With. — New Phytol. 81: 331–339, 1978.

    Article  CAS  Google Scholar 

  • Baker, A.J.M.: Accumulators and excluders-strategies in the response of plants to heavy metals. — J. Plant Nutr. 3: 643–654, 1981.

    Article  CAS  Google Scholar 

  • Baker, A.J.M., Brooks, R.R.: Terrestrial higher plants which hyper accumulate metallic elements — review of their distribution, ecology and phytochemistry. — Biorecovery 1: 81–126, 1989.

    CAS  Google Scholar 

  • Baker, A.J.M., Walker, P.L.: Ecophysiology of metal uptake by tolerant plants: heavy metal tolerance in plants. — In: Shaw, A.J. (ed.): Heavy Metal Tolerance in Plants: Evolutionary Aspects. Pp. 155–177. CRC Press, Boca Raton, 1990.

    Google Scholar 

  • Balakhnina, T., WŁodarczyk, T., Borkowska, A., Nosalewicz, N., Serdyuk, O., Smolygina, L., Ivanova, E., Fomina, I.: Effect of 4-hydroxyphenethyl alcohol on growth and adaptive potential of barley plants under optimal and soil flooding conditions. — Polish J. environ. Stud. 19: 565–572, 2009.

    Google Scholar 

  • Baranowska-Morek, A., Wierzbicka, M.: Localization of lead in root tip of Dainthus carthusianorum. — Acta biol. cracow. Ser. Bot. 46: 45–56, 2004.

    Google Scholar 

  • Barbafieri, M., Tassi, E.: Brassinosteroids for phytoremediation application. — In: Hayat, S., Ahmad, A. (ed.): Brassinosteroids: a Class of Plant Hormones. Pp. 403–437. Springer, Berlin 2011.

    Chapter  Google Scholar 

  • Bareen, M.S., Jamil, S.: Role of plant growth regulators and a saprobic fungus in enhancement of metal phytoextraction potential and stress alleviation in pearl millet. — J. hazard. Mater. 237–238: 186–193, 2012.

    Article  Google Scholar 

  • Brooks, R.R., Lee, J., Jaffré, T.: Some New Zealand and New Caledonian plant accumulators of nickel. — J. Ecol. 62: 493–499, 1974.

    Article  CAS  Google Scholar 

  • Cassina, L., Tassi, T., Pedron, F., Petruzzelli, G., Ambrosini, P., Barbafieri, M.: Using a plant hormone and a thioligand to improve phytoremediation of Hg-contaminated soil from a petrochemical plant. — J. hazard. Mater. 231–232: 36–42, 2012.

    Article  PubMed  Google Scholar 

  • Chen, C.Y., Zou, J.H., Zhang, S.Y., Zaitlin, D., Zhu, L.H.: Stringolactones are a new-defined class of plant hormones which inhibit shoot branching and mediate the interaction of plant-AM fungi and plant-parasitic weeds. — Sci. China Ser. C 52: 693–700, 2009.

    Article  CAS  Google Scholar 

  • Cunningham, S.D., Berti, W.R.: Remediation of contaminated soils with green plants: an overview. — In Vitro cell. dev. Biol. Plant 29: 207–212, 1993.

    Article  Google Scholar 

  • Du, R.J., He, E.K., Tang, Y.T., Hy, P.J., Ying, R.R., Morel, J.L., Qiu, R.L.: How phytohormone IAA and chelator EDTA affect lead uptake by Zn/Cd hyperaccumulator Picris divaricata. — Int. J. Phytoremed. 13: 1024–1036, 2011.

    Article  CAS  Google Scholar 

  • Evangelou, M.H.W., Ebel, M., Schaeffer, A.: Evaluation of the effect of small organic acids on phytoextraction of Cu and Pb soil with tobacco Nicotiana tabacum. — Chemosphere 63: 996–1004, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Evangelou, M.W.H., Ebel, M., Schaeffer, A.: Chetale assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. — Chemophere 68: 989–1003, 2007.

    Article  CAS  Google Scholar 

  • Fuentes, H.D., Khoo, C.S., Pe, T., Muir, S., Khan, A.G.: Phytoremediation of a contaminated mine site using plant growth regulators to increase heavy metal uptake. — In: Sánchez, M. (ed.): Proceedings of the 5th International Conference on Clean Technologies for the Mining Industry. Vol. 1. Pp. 427–435. Universidad de Concepción, Santiago 2000.

    Google Scholar 

  • Gawronski, S.W., Greger, M., Gawronska, H.: Plant taxonomy and metal phytoremediation. — In: Sherameti, I., Varma, A. (ed.): Detoxification of Heavy Metals. Pp. 91–109. Springer, Berlin — Heidelberg 2011.

    Chapter  Google Scholar 

  • Gosh, M., Singh, S.P.: A review of phytoremediation of heavy metals and utilization of its byproducts. — Appl. Ecol. Environ. Res. 3: 1–18, 2005.

    Google Scholar 

  • Hadi, F., Bano, A., Fuller, M.P.: The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. — Chemosphere 80: 457–462, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Hajiboland, R., Manafi, M.H.: Flora of heavy metal-rich soils in NW Iran and some potential hyper-accumulator and accumulator species. — Acta bot. croat. 66: 177–195, 2007.

    CAS  Google Scholar 

  • Huang, J.W., Blaylock, M.J., Kapulnik, Y., Ensley, B.D.: Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. — Environ. Sci. Technol. 32: 2004–2008, 1998.

    Article  CAS  Google Scholar 

  • Israr, M., Jewell, A., Kumar, D., Sahi, S.V.: Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of S. drummondii. — J. hazard. Mater. 186: 1520–1526, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Jones, D.L., Darrah, P.R.: Influx and efflux of organic acids across the soil-root interface of Zea mays L. and its implications in rhizosphere C flow. — Plant Soil 173: 103–109, 1995.

    Article  CAS  Google Scholar 

  • Kabata-Pendias A.: Trace Elements in Soils and Plants. — CRC Press, Boca RAton — London — New York 2011.

    Google Scholar 

  • Kamal, M., Ghaly, A.E., Mahmoud, N., Côte, R.: Phytoaccumulation of heavy metals by aquatic plants. — Environ. Int. 29: 1029–1039, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Kozlov, M.V., Haukioja E., V., Bakhtiarov, A.V., Stroganov D.N.: Heavy metals in birch leaves around a nickel-copper smelter at Monchegorsk, Northwestern Russia. — Environ. Pollut. 90: 291–299, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Khan, A.S., Chaudhry, N.Y.: GA3 improves flower yield in some cucurbits treated with lead and mercury. — Afr. J. Biotechnol. 5: 149–153, 2006.

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Liphadzi, M.S., Kirkham, M.B., Paulsen, G.M.: Auxinenhanced root growth for phytoremediation of sewagesludge amended soil. — Environ. Technol. 27: 695–704, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Lipiec, J.: Crop responses to soil compaction. — Nordic Assoc. agr. Sci. Rep. 8: 32, 2012.

    Google Scholar 

  • Liu, D., Li, T., Yang, X., Islam, E., Jin, X., Mahmood, Q.: Enhancement of lead uptake by hyperaccumulator plant species Sedum alfredii Hance using EDTA and IAA. — Bull. Environ. Contam. Toxicol. 78: 280–283, 2007.

    Article  CAS  PubMed  Google Scholar 

  • López, M.L., Peralta-Videa, J.R., Benitez, T., Gardea-Torresdey, J.L.: Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. — Chemosphere 61: 595–598, 2005.

    Article  PubMed  Google Scholar 

  • López-Bucio, J., Nieto-Jacobo, M.F., Ramírez-Rodríguez, V., Herrera-Estrella, L.: Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. — Plant Sci. 160: 1–13, 2000.

    Article  PubMed  Google Scholar 

  • Machackova, I., Zazimalova, E., George, E.F.: Plant growth regulators I: Introduction; auxins, their analogues and inhibitors. — In: George, E.F., Hall, M.A., De Klerk, G.-J. (ed.): Plant Propagation by Tissue Culture. Pp. 175–183. Springer, Berlin 2008.

    Google Scholar 

  • Martin, S.R., Llugany, M., Barceló, J., Poschenrieder, C.: Cadmium exclusion a key factor in differential Cdresistance in Thlaspi arvense ecotypes. — Biol. Plant. 56: 729–734, 2012.

    Article  CAS  Google Scholar 

  • Masarovičová E., Králová K., Kummerová M.: Principles of classification of medical plants as hyperaccumulators or excluders. — Acta Physiol. Plant. 32: 823–829, 2010.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mganga, N., Manoko, M.L.K., Rulangaranga, Z.K.: Classification of plants according to their heavy metal content around North Mara gold mine, Tanzania: implication for phytoremediation. — Tanz. J. Sci. 37: 109–119, 2011.

    Google Scholar 

  • Miransari, M.: Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. — Biotechnol. Adv. 29: 645–653, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ouzounidou, G., Ilias, I.: Hormone-induced protection of sunflower photosynthetic apparatus against copper toxicity. — Biol. Plant. 49,2: 233–228, 2005.

    Article  Google Scholar 

  • Padmavathiamma, P.K., Li, L.Y.: Phytoremediation technology: hyper-accumulation metals in plants. — Water Air Soil Pollut. 184: 105–126, 2007.

    Article  CAS  Google Scholar 

  • Pilon-Smiths, E.A.H., Quinn, C.F., Tapken, W., Malagoni, M., Schiavon, M.: Physiological functions of beneficial elements. — Curr. Opin. Plant. Biol. 12: 267–274, 2009.

    Article  Google Scholar 

  • Piotrowska, A., Bajguz, A., Godlewska-Żyłkiewicz, B., Czerpak, R., Kamińska, M.: Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). — Environ. exp. Bot. 66: 509–513, 2009.

    Article  Google Scholar 

  • Pospíšilová, J., Synková, H., Rulcová, J.: Cytokinins and water stress. — Biol. Plant. 43: 321–328, 2000.

    Article  Google Scholar 

  • Sanitá Di Toppi, L., Gabrielli, R.: Response to cadmium in higher plants. — Environ. exp. Bot. 41: 105–130, 1999.

    Article  Google Scholar 

  • Santos, J.A.G., Gonzaga, M.I.S., Ma, L.Q., Srivastava, M.: Timing of phosphate application affects arsenic phytoextraction by Pteris vittata L. of different ages. — Environ. Pollut. 154: 306–311, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Sarma, H.: Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. — J. Environ. Sci. Technol. 4: 118–138, 2011.

    Article  CAS  Google Scholar 

  • Sarret, G., Vangronsveld, J., Manceau, A., Musso, M., D’Hean, J., Menthonnex, J.J., Hazemann, J.L.: Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. — Environ. Sci. Technol. 35: 2854–2859, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Sarret, G., Harada, E., Choi, Y.E., Isaure, M.P., Geoffroy, N., Fakara, S., Marcus, M.A., Birschwilks, M., Clemens, S., Manceau, A.: Trichomes of tobacco excrete zinc as zincsubstituted calcium carbonate and other zinc-containing compounds. — Plant Physiol. 141: 1021–1034, 2006.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh, A., Kuhad, R.C., Ward, O.P.: Biological remediation of soil: an overview of global market and available technologies. — In: Singh, A., Kuhad, R.C., Ward, O.P. (ed.): Advances in Applied Bioremediation. Vol. 17. Pp. 1–19, Springer-Verlag, Berlin — Heidelberg 2009.

    Chapter  Google Scholar 

  • Szarek-Łukaszewska, G., Słysz, A., Wierzbicka, M.: Response to Armeria maritima (Mill.) Willd. to Cd, Zn and Pb. — Acta biol. cracov. Ser. Bot. 46: 19–24, 2004.

    Google Scholar 

  • Tassi, E., Pedron, F., Barbafieri, M., Petruzelli, G.: Phosphateassisted phytoremediation in As-contaminated soil. — Eng. Life Sci. 4: 341–346, 2004.

    Article  CAS  Google Scholar 

  • Tassi, E., Pouget, J., Petruzzelli, G., Barbafieri, M.: The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. — Chemosphere 71: 66–73, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Tian, S.K., Lu, L.L., Yang, X.E., Huang, H.G., Wang, K., Brown, P.H.: Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii. — Biol. Plant. 56: 344–350, 2012.

    Article  CAS  Google Scholar 

  • Tu, S., Ma, L.Q., MacDonald, G.E., Bondada, B.: Effects of arsenic and phosphorus on arsenic absorption, arsenate reduction and thiol formation in excised parts of Pteris vittata L. — Environ. exp. Bot. 51: 121–131, 2004.

    Article  CAS  Google Scholar 

  • Vamerali, T., Bandiera, M., Hartley, W., Carletti, P., Mosca, G.: Assisted phytoremediation of mixed metal(loid)-polluted pyrite waste: effects of foliar and substrate IBA application on fodder radish. — Chemosphere 84: 213–219, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Van Nevel, L., Mertens, J., Verheyen, K.: Phytoextraction of metals from soils: how far from practice? — Environ. Pollut. 150: 34–40, 2007.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vogel-Mikuš, K., Drobne, D., Regvar, M.: Zn, Cd and Pb accumulation and arbuscural mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. — Environ. Pollut. 133: 233–242, 2005.

    Article  PubMed  Google Scholar 

  • Wang, H., Shan, X., Wen, B., Owens, G., Fang, J., Zhang, S.: Effects of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. — Environ. exp. Bot. 61: 246–253, 2007.

    Article  CAS  Google Scholar 

  • Wang, J., Zhao, F.J., Meharg, A.A., Raab, A., Fieldmann, J., McGrath, S.P.: Mechanisms of arsenic hyperaccumulation in Pteris vittata. — Plant Physiol. 130: 1552–1561, 2002.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu, H.B., Tang, R.R.: Using elevated CO2 to increase the biomass of a Sorghum vulgare × Sorgum vulgare var. sudanense hybrid and Trifolium pretense L. and to trigger hyperaccumulation of cesium. — J. hazard. Mater. 170: 861–870, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Yang, X., Feng, Y., He, Z., Stoffella, P.J.: Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. — J. Trace Element med. Biol. 18: 339–353, 2005.

    Article  CAS  Google Scholar 

  • Yuan, Z., Van Briesen, J.M.: The formation of intermediates in EDTA and NTA biodegradation. — Environ. Eng. Sci. 23: 533–544, 2006.

    Article  CAS  Google Scholar 

  • Zenk, M.H.: Heavy metal detoxification in higher plants: a review. — Gene 179: 21–30, 1996.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Bulak.

Additional information

Acknowledgments: The authors would like to thank an anonymous reviewer for valuable comments and for the work he has put into creating the review. This paper was partly financed from the funds of the National Centre for Research and Development in Poland in the frame of the project: Knowledge Hub FACCE JPI “Modelling European Agriculture with Climate Change for Food Security” (MACSUR, P162).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bulak, P., Walkiewicz, A. & Brzezińska, M. Plant growth regulators-assisted phytoextraction. Biol Plant 58, 1–8 (2014). https://doi.org/10.1007/s10535-013-0382-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-013-0382-5

Additional key words

Navigation