Skip to main content
Log in

Morphoanatomical responses induced by excess iron in roots of two tolerant grass species

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

We aimed to verify whether morphoanatomic alterations occur in response to excess iron, in roots of Setaria parviflora and Paspallum urvillei (Poaceae), and to localize the presence of the sites of iron accumulation. Plants were subjected to 0.009, 1, 2, 4, and 7 mM Fe-EDTA in nutrient solution. Both species presented iron contents in the roots above the critical toxicity level. The presence of iron plaque on roots of the two species was confirmed, and it may have reduced iron absorption by the plants. Roots from the two species showed typical visual symptoms of stress by excess iron: change in color and mucilaginous and flaccid appearance. Anatomical damage was observed in both species: aerenchyma disruption, alterations in endodermal cells, and irregular shape of both vessel and sieve tube elements. The metal was histolocalized in the cortex and in protoxylem and metaxylem cell walls in both species, which suggests a detoxification strategy for the excess iron. Phenolic compounds were not histolocalized in roots. Microscopic analyses were therefore effective in evaluating the real damage caused by excess iron.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adamski JM, Danieloski R, Deuner S, Braga EJB, Castro LAS, Peters JA (2012) Responses to excess iron in sweet potato: impacts on growth, enzyme activities, mineral concentrations, and anatomy. Acta Physiol Plant 34:1827–1836

    Article  CAS  Google Scholar 

  • Araújo TO, Freitas-Silva L, Santana BVN, Kuki KN, Pereira EG, Azevedo AA, Silva LC (2014) Tolerance to iron accumulation and its effects on mineral composition and growth of two grass species. Environ Sci Pollut Res 21:2777–2784

    Article  Google Scholar 

  • Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil 201:137–147

    Article  CAS  Google Scholar 

  • Briat J, Ravet K, Arnaud N, Duc C, Boucherez J, Touraine B, Cellier F, Gaymard F (2010) New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot Lond 105:811–822

    Article  CAS  Google Scholar 

  • Chen CC, Dixon JB, Turner FT (1980) Iron coatings on rice roots: morphology and models of development. Soil Sci Soc Am J 44:1113–1119

    Article  CAS  Google Scholar 

  • Ducic T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Braz J Plant Physiol 17:103–112

    Article  CAS  Google Scholar 

  • Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49

    Article  Google Scholar 

  • Fontes PCR (2006) Diagnosis of Nutritional Status of Plants.Viçosa: UFV (In Portuguese)

  • Giampaoli P, Tresmondi F, Lima GPP, Kanashiro S, Alves ES, Domingos M, Tavares AR (2012) Analysis of tolerance to copper and zinc in Aechmea blanchetiana grown in vitro. Biol Plant 56:83–88

    Article  CAS  Google Scholar 

  • Gomes MP, Carvalho M, Marques TCLLSM, Duarte DM, Nogueira COG, Soares AM, Garcia QS (2012) Arsenic-sensitivity in Anadenanthera peregrina due to arsenic-induced lipid peroxidation. Int J Appl Sci Technol 2:55–63

  • Hecht-Buchholz C (1983) Light and electron microscopic investigations of the reactions of various genotypes to nutritional disorders. Plant Soil 72:151–165

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station, Berkeley

  • Jiang FY, Chen X, Luo AC (2009) Iron plaque formation on wetland plants and its influence on phosphorus, calcium and metal uptake. Aquat Ecol 43:879–890

    Article  CAS  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. Mc Graw Hill, New York

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Liu J, Leng X, Wang M, Zhu Z, Dai Q (2011) Iron plaque formation on roots of different rice cultivars and the relation with lead uptake. Ecotoxicol Environ Saf 74:1304–1309

    Article  CAS  Google Scholar 

  • Lux A, Sottnikova A, Opatrna J, Greger M (2004) Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol Plant 120:537–545

    Article  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculík M, White PJ (2010) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  Google Scholar 

  • Macnair MR (1993) Tansley Review No. 49: the genetics of metal tolerance in vascular plants. New Phytol 124:541–559

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plant. Academic, NewYork

    Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530

    CAS  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot Lond 102:3–13

    Article  CAS  Google Scholar 

  • Nozoye N, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454

    Article  CAS  Google Scholar 

  • O'Brien TP, Mccully ME (1981) The study of plant structure principles and selected methods, Melbourne, Termarcarphi Pty. Ltd

  • Pereira EG, Oliva MO, Rosado-Souza L, Mendes GC, Colares DS, Stopato CH, Almeida AM (2013) Iron excess affects rice photosynthesis through stomatal and non-stomatal limitations. Plant Sci 201–202:81–92

    Article  Google Scholar 

  • Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Fe homeostasis in plant cells: does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration? Planta 213:967–76

    Article  CAS  Google Scholar 

  • Sant’Anna-Santos BF, Azevedo AA (2007) Aspectos morfoanatômicos da fitotoxidez do flúor em duas espécies tropicais. Rev Bras Biochem 5:48–50

    Google Scholar 

  • Sant’Anna-Santos BF, Silva LC, Azevedo AA, Araújo JM, Alves EF, Silva AM, Aguiar RM (2006) Effects of simulated acid rain on the foliar micromorphology and anatomy of tree tropical species. Environ Exp Bot 58:158–168

    Article  Google Scholar 

  • Santana BVN, Araújo TO, Andrade GC, Freitas-Silva L, Kuki KN, Pereira EG, Azevedo AA, Silva LC (2014) Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential. Environ Sci Pollut Res 21:2550–2562

    Article  CAS  Google Scholar 

  • Seyfferth A, Webb SM, Andrews JC, Fendorf S (2010) Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environ Sci Technol 44:8108–8113

    Article  CAS  Google Scholar 

  • Silva LC, Azevedo AA, Silva EAM, Oliva MA (2000) Flúor em chuva simulada: sintomatologia e efeitos sobre a estrutura foliar e o crescimento de plantas arbóreas. Rev Bras Bot 23:383–391

    Google Scholar 

  • Silva LC, Oliva MA, Azevedo AA, Araújo JM, Aguiar RM (2005) Micromorphological and anatomical alterations caused by simulated acid rain in restinga plants: Eugenia uniflora and Clusia hilariana. Water Air Soil Pollut 168:129–143

    Article  CAS  Google Scholar 

  • Silva LC, Oliva MA, Azevedo AA, Araújo JM (2006) Responses of restinga plant species to pollution from an iron pelletization factory. Water Air Soil Pollut 175:241–256

    Article  Google Scholar 

  • Sinha S, Gupta M, Chandra P (1997) Oxidative stress induced by iron in Hydrilla verticillata (l.f.) royle: response of antioxidants. Ecotoxicol Environ Saf 38:286–291

    Article  CAS  Google Scholar 

  • Siqueira-Silva AI, Silva LC, Azevedo AA, Oliva MA (2012) Iron plaque formation and morphoanatomy of roots from species of resting subjected to excess iron. Ecotoxicol Environ Saf 78:265–275

    Article  CAS  Google Scholar 

  • Stephan UW (2002) Intra- and intercellular iron trafficking and subcellular compartmentation within roots. Plant Soil 241:19–25

    Article  CAS  Google Scholar 

  • Stevens A, Chalk BT (1996) Pigments and minerals. In: Bancroft JD, Stevens A (eds) Theory and practice of histological techniques, 4th edn. Churchill Livingstone, New York, pp 243–267

    Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    Article  CAS  Google Scholar 

  • Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70:1254–1257

    Article  CAS  Google Scholar 

  • Tsai T, Huang H (2006) Effects of iron excess on cell viability and mitogen-activated protein kinase activation in rice roots. Physiol Plant 127:583–592

    Article  CAS  Google Scholar 

  • Wang ZY, Liu LH, Wen SF, Peng CS, Xing BS, Li FM (2010) Effect of iron plaque on root surfaces on phosphorus uptake of two wetland plants. Coll Environ Sci Eng 31:781–786

    Google Scholar 

  • Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. BBA Biomembr 1465:104–126

    Article  CAS  Google Scholar 

  • Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892

    Article  CAS  Google Scholar 

  • Zhang X, Zhang F, Mao D (1999) Effect of iron plaque outside roots on nutrient uptake by rice (Oryza sativa L.): phosphorus uptake. Plant Soil 209:187–192

    Article  CAS  Google Scholar 

  • Zhong S, Shi J, Xu J (2010) Influence of iron plaque on accumulation of lead by yellow flag (Iris pseudacorus L.) grown in artificial Pb-contaminated soil. J Soil Sediment 10:964–970

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the approval of a PNADB Project (Programa Nacional de Apoio e Desenvolvimento da Botânica); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the approval of a SISBIOTA-BRASIL (proc. CNPq 563335/2010-6; proc. FAPESP 2010/52319-6) Project and for the Research Productivity Scholarships granted to L.C. Silva (309170/2012-5) and A.A. Azevedo (307538/2010-9); Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the approval of projects CRA-APQ-01361-12 and RDP–00195-10; Secretaria de Estado de Ciência, Tecnologia e Ensino Superior (SECTES) and Projeto Floresta Escola, for financial support; Hilda Maria Longhi Wagner, for species identification; and Núcleo de Microscopia e Microanálise of Universidade Federal de Viçosa (UFV).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luzimar Campos da Silva.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Araújo, T.O., de Freitas-Silva, L., Santana, B.V.N. et al. Morphoanatomical responses induced by excess iron in roots of two tolerant grass species. Environ Sci Pollut Res 22, 2187–2195 (2015). https://doi.org/10.1007/s11356-014-3488-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3488-1

Keywords

Navigation