Abstract
One of the industrial pillars of Espírito Santo state, South East of Brazil, is iron-mining products processing. This activity brings to a high level of coastal pollution due to deposition of iron particulate on fragile ecosystems as mangroves and restinga. Schinus therebinthifolius (aroeira) is a widespread restinga species. This work tested iron toxicity alleviation by vermicompost humic substances (HS) added to aroeira seedlings in hydroponic conditions. Catalase, peroxidase, and ascorbate peroxidase are antioxidant enzymes that work as reactive oxygen species (ROS) scavengers: they increase their activity as an answer to ROS concentration rise that is the consequence of metal accumulation or humic substance stimulation. S. terebinthifolius seedlings treated with HS and Fe augmented their antioxidant enzyme activities significantly less than seedlings treated separately with HS and Fe; their significantly lower Fe accumulation and the slight increase of root and leaf area confirm the biostimulating effect of HS and their role in blocking Fe excess outside the roots. The use of HS can be useful for the recovery of areas contaminated by heavy metals.
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References
Aguiar NO, Canellas LP, Dobbss LB, Zandonadi DB (2009) Distribuição de massa molecular e bioatividade de ácidos húmicos. Rev Bras Ciênc Solo 33(6):1613–1623. https://doi.org/10.1590/S0100-06832009000600010
Aguiar NO, Medici LM, Olivares FL, Dobbss LB, Torres-Netto A, Silva SF, Novotny EH, Canellas LP (2016) Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann Appl Biol 168(2):203–213. https://doi.org/10.1111/aab.12256
Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109(4):1247–1257. https://doi.org/10.1104/pp.109.4.1247
Arrivabene HP, Souza IC, Co WLO, Conti MM, Wunderlin DA, Milanez CRD (2015) Effect of pollution by particulate iron on the morphoanatomy, histochemistry, and bioaccumulation of three mangrove plant species in Brazil. Chemosphere 127:27–34. https://doi.org/10.1016/j.chemosphere.2015.01.011
Arrivabene HP, Campos CQ, Souza IC, Wunderlin DA, Milanez CRD, Machado SR (2016) Differential bioaccumulation and translocation patterns in three mangrove plants experimentally exposed to iron. Consequences for environmental sensing. Environ Pollut 215:302–313. https://doi.org/10.1016/j.envpol.2016.05.019
Bandiera M, Mosca G, Vamerali T (2009) Humic acids affect root characteristics of fodder radish (Raphanus sativus L. var. oleiformis Pers.) in metal-polluted wastes. Desalination 246(1-3):78–91. https://doi.org/10.1016/j.desal.2008.03.044
Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron dependent free radical generation in plants subjected in environmental stress: toxicity and antioxidant protection. Plant Soil 201(1):137–147. https://doi.org/10.1023/A:1004375732137
Briat JF, Cellier F, Gaymard F (2006) Ferritins and iron accumulation in plant tissues. In: Barton LL, Abadía J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, New York, pp 341–357. https://doi.org/10.1007/1-4020-4743-6_17
Busato JG, Zandonadi DB, Souza IM, Marinho EB, Dobbss LB, Mol1 AR (2016) Efeito do extrato húmico solúvel em água e biofertilizante sobre o desenvolvimento de mudas de Callophyllum brasiliense. Pesq flor bras 36(86):161–168
Cacco G, Dell’Agnola G (1984) Plant growth regulator activity of soluble humic complex. Can J Soil Sci 62(2):306–310. https://doi.org/10.4141/cjss84-023
Canellas LP, Olivares FO (2014) Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric 1(3):1–11. https://doi.org/10.1186/2196-5641-1-3
Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957
Canellas LP, Piccolo A, Dobbss LB, Spaccini R, Olivares FL, Zandonadi DB, Façanha AR (2010) Chemical composition and bioactivity properties of size-fractions separated from a vermicompost humic acid. Chemosphere 78:457–466
Canellas LP, Dobbss LB, Oliveira AL, Chagas JG, Aguiar NO, Rumjanekc VM, Novotny EH, Olivares FL, Spaccini R, Piccolo A (2012) Chemical properties of humic matter as related to induction of plant lateral roots. Eur J Soil Sci 63:315–324
Canellas LP, Olivares FL, Aguiar NO, Jones DL, Nebbioso A, Mazzei P, Piccolo A (2015) Humic and fulvic acids as biostimulants in horticulture. Sci Hortic 196:15–27. https://doi.org/10.1016/j.scienta.2015.09.013
Cardwell RD, Deforest DK, Brix KV, Adams WJ (2013) Do Cd, Cu, Ni, Pb, and Zn biomagnify in aquatic ecosystems? Rev Environ Contam Toxicol 226:101–122. https://doi.org/10.1007/978-1-4614-6898-1_4
Cheng H, Wang M, Wong MH, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375(1-2):137–148. https://doi.org/10.1007/s11104-013-1945-0
Cordeiro FC, Santa-Catarina C, Silveira V, de Souza SR (2011) Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea Mays L.) Biosci Biotechnol Biochem 75(1):70–74. https://doi.org/10.1271/bbb.100553
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:1–13. https://doi.org/10.3389/fenvs.2014.00053
Dobbss LB, Medici LO, Peres LE, Pino-Nunes LE, Rumjanek VM, Façanha AR, Canellas LP (2007) Changes in root development of Arabidopsis promoted by organic matter from oxisols. Ann Appl Biol 151:199–211
Dobbss LB, Canellas LP, Olivares FL, Aguiar NO, Peres LEP, Azevedo M, Spaccini R, Piccolo A, Façanha AR (2010) Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J Agric Food Chem 58(6):3681–3688. https://doi.org/10.1021/jf904385c
Dobbss LB, Barroso ALP, Ramos AC, Torrico KSN, Arçari FSS, Zandonadi DB (2016) Bioactivity of mangrove humic materials on Rizophora mangle and Laguncularia racemosa seedlings, Brazil. Afr J Biotechnol 15(23):1168–1176
Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on the univalent cations. Annu Rev Plant Physiol 17(1):47–76. https://doi.org/10.1146/annurev.pp.17.060166.000403
Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21. https://doi.org/10.1016/j.phytochem.2014.07.020
García AC, Santos LA, Souza LGA, Tavares OCH, Zonta E, Gomes ETM, García-Mina JM, Berbara RLL (2016) Vermicompost humic acids modulate the accumulation and metabolism of ROS in rice plants. J Plant Physiol 192:56–63. https://doi.org/10.1016/j.jplph.2016.01.008
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Greipsson S (1994) Effects of iron plaque on roots of rice on growth and metal concentration of seeds and plant tissues when cultivated in excess copper. Commun Soil Sci Plant Anal 25(15-16):2761–2769. https://doi.org/10.1080/00103629409369223
Greipsson S, Crowder AA (1992) Amelioration of copper and nickel toxicity by iron plaque on roots of rice (Oryza sativa). Can J Bot 70(4):824–830. https://doi.org/10.1139/b92-105
Haghighi M, Kafi M, Fang P, Gui-Xiao L (2010) Humic acid decreased hazardous of cadmium toxicity on lettuce (Lactuca sativa L.). Veg. Crops. Res Bull 72:49–61
Halliwell B, Gutteridge JMC (1984) Oxigen toxicity, oxygen radicals, transition metals and disease. Biochem J 219(1):1–4. https://doi.org/10.1042/bj2190001
Hattab N, Soubrand M, Guegan R, Motelica-Heino M, Bourrat X, Faure O, Bouchardon JL (2014) Effect of organic amendments on the mobility of trace elements in phytoremediated techno-soils: role of the humic substances. Environ Sci Pollut Res 21(17):10470–10480. https://doi.org/10.1007/s11356-014-2959-8
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450
Hohmann I, Bill R, Kayingo I, Prior B (2000) Microbial MIP channels. Trends Microbiol 8(1):33–38
Hossain MA, Piyatida P, 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. J Bot 37:1–37. https://doi.org/10.1155/2012/872875
Instituto Brasileiro de Mineração - IBRAM (2015) Informações sobre a economia mineral brasileira. IBRAM, Belo Horizonte 25p
Kaldenhoff R, Fischer M (2006) Functional aquaporin diversity in plants. BBA-Biomembr 1758(8):1134–1141. https://doi.org/10.1016/j.bbamem.2006.03.012
Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57(2):315–319. https://doi.org/10.1104/pp.57.2.315
Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32. https://doi.org/10.1016/j.phytochem.2014.09.016
Krohling CA, Eutrópio FJ, Bertolazi AA, Dobbss LB, Campostrini E, Dias T, Ramos AC (2016) Ecophysiology of iron homeostasis in plants. Soil Sci Plant Nutr 62(1):39–47. https://doi.org/10.1080/00380768.2015.1123116
Kuki KN, Oliva MA, Pereira EG (2008) Iron ore industry emissions as a potential ecological risk factor for tropical coastal vegetation. Environ Manag 42(1):111–121. https://doi.org/10.1007/s00267-008-9093-7
Kuki KN, Oliva MA, Costa AC (2009) The simulated effects of iron dust and acidity during the early stages of establishment of two coastal plant species. Water Air Soil Pollut 196(1–4):287–295. https://doi.org/10.1007/s11270-008-9776-y
Lagier T, Feuillade G, Matejka G (2000) Interactions between copper and organic macromolecules: determination of conditional complexation constants. Agronomie 20(5):537–546. https://doi.org/10.1051/agro:2000148
Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Iron. In: Mengel K, Kirkby E (eds) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht, pp 553–571. https://doi.org/10.1007/978-94-010-1009-2_13
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nardi S, Pizzeghello D, Schiavon M, Ertani A (2016) Plant biostimulants: physiological responses induced by protein hydrolyzed-based. Sci Agric 73(1):18–23. https://doi.org/10.1590/0103-9016-2015-0006
Nath B, Chaudhuri P, Birch G (2014) Assessment of biotic response to heavy metal contamination in Avicennia marina mangrove ecosystems in Sydney estuary, Australia. Ecotoxicol Environ Saf 107:284–290. https://doi.org/10.1016/j.ecoenv.2014.06.019
Nica DV, Bura M, Gergen I, Harmanescu M, Bordean DM (2012) Bioaccumulative and conchological assessment of heavy metal transfer in a soil plant-snail food chain. Chem Cent J 6(1):1–15. https://doi.org/10.1186/1752-153X-6-55
Peixoto PHP, Cambraia J, Sant’Anna R, Mosquim PR, Moreira MA (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal 11:137–143
Pinto SS, Souza AE, Oliva MA, Pereira EG (2016) Oxidative damage and photosynthetic impairment in tropical rice cultivars upon. Sci Agric 73(3):217–226. https://doi.org/10.1590/0103-9016-2015-0288
Polle A, Schützendübel A (2003) Heavy metal signalling in plants: linking cellular and organismic responses. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress. Springer, Berlin, pp 187–215
Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Phisiol 127(3):887–898
Sergiev I, Todorova D, Moskova I, Georgieva N, Nikolova A, Simova S, Polizoev D, Alexieva V (2013) Protective effect of humic acids against heavy metal stress in triticale. Compt Acad Sci 66:53–60
Sung K, Kim KS, Park S (2013) Enhancing degradation of total petroleum hydro-carbons and uptake of heavy metals in a wetland microcosm planted with Phrag-mites communis by humic acids addition. Int J Phytoremediation 15(6):536–549. https://doi.org/10.1080/15226514.2012.723057
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(4):985–999. https://doi.org/10.1007/s11738-012-1169-6
Wang Q, Zhu L, Cheng S, Zhenbin WZ (2010) Effects of humic acids on phytoextraction of Cu and Cd from sediment by Elodea nuttallii. Chemosphere 78(5):604–608. https://doi.org/10.1016/j.chemosphere.2009.11.011
Wiszniewska A, Hanus-Fajerska E, Muszynska E, Ciarkowska K (2016) Natural organic amendments for improved phytoremediation of polluted soils: a review of recent progress. Pedosphere 26(1):1–12. https://doi.org/10.1016/S1002-0160(15)60017-0
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76(2):167–179. https://doi.org/10.1016/j.sajb.2009.10.007
Zakikhani H, Ardakani MR, Rejali F, Gholamhoseini M, Joghan AK, Dolatabadian A (2012) Influence of diazotrophic bacteria on antioxidant enzymes and some biochemical characteristics of soybean subjected to water stress. J Integr Agric 11(11):1828–1835. https://doi.org/10.1016/S2095-3119(12)60187-7
Zandonadi DB, Canellas LP, Façanha AR (2007) Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225(6):1583–1595. https://doi.org/10.1007/s00425-006-0454-2
Zandonadi DB, Santos MP, Dobbss LB, Olivares FL, Canellas LP, Binzel ML, Okorokova-Façanha AL, Façanha AR (2010) Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta 231:1025–1036
Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 47:157–164
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Authors thank Dr. Pitolas Armini for the map of ports and the seed collection area, to FAPES—Fundação de Amparo à Pesquisa do Espírito Santo for the scholarship granted for the project, to University Vila Velha (UVV), and to the National Council of Technological and Scientific Development.
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Dobbss, L.B., dos Santos, T.C., Pittarello, M. et al. Alleviation of iron toxicity in Schinus terebinthifolius Raddi (Anacardiaceae) by humic substances. Environ Sci Pollut Res 25, 9416–9425 (2018). https://doi.org/10.1007/s11356-018-1193-1
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DOI: https://doi.org/10.1007/s11356-018-1193-1