Iron toxicity resistance strategies in tropical grasses:The role of apoplastic radicular barriers
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摘要
The revegetation of mined areas poses a great challenge to the iron ore mining industry.The initial recovery process in degraded areas might rely on the use of Fe-resistant grasses.Tropical grasses, such as Paspalum densum and Echinochloa crus-galli, show different resistance strategies to iron toxicity; however, these mechanisms are poorly understood.The Fe-resistance mechanisms and direct iron toxicity as a function of root apex removal were investigated. To achieve this purpose, both grass species were grown for up to 480 hr in a nutrient solution containing 0.019 or 7 mmol/L Fe-EDTA after the root apices had been removed or maintained. Cultivation in the presence of excess iron-induced leaf bronzing and the formation of iron plaque on the root surfaces of both grass species, but was more significant on those plants whose root apex had been removed. Iron accumulation was higher in the roots, but reached phytotoxic levels in the aerial parts as well. It did not hinder the biosynthesis of chloroplastidic pigments. No significant changes in gas exchange and chlorophyll a fluorescence occurred in either grass when their roots were kept intact; the contrary was true for plants with excised root apices. In both studied grasses, the root apoplastic barriers had an important function in the restriction of iron translocation from the root to the aerial plant parts, especially in E. crus-galli. Root apex removal negatively influenced the iron toxicity resistance mechanisms(tolerance in P. densum and avoidance in E. crus-galli).
The revegetation of mined areas poses a great challenge to the iron ore mining industry.The initial recovery process in degraded areas might rely on the use of Fe-resistant grasses.Tropical grasses, such as Paspalum densum and Echinochloa crus-galli, show different resistance strategies to iron toxicity; however, these mechanisms are poorly understood.The Fe-resistance mechanisms and direct iron toxicity as a function of root apex removal were investigated. To achieve this purpose, both grass species were grown for up to 480 hr in a nutrient solution containing 0.019 or 7 mmol/L Fe-EDTA after the root apices had been removed or maintained. Cultivation in the presence of excess iron-induced leaf bronzing and the formation of iron plaque on the root surfaces of both grass species, but was more significant on those plants whose root apex had been removed. Iron accumulation was higher in the roots, but reached phytotoxic levels in the aerial parts as well. It did not hinder the biosynthesis of chloroplastidic pigments. No significant changes in gas exchange and chlorophyll a fluorescence occurred in either grass when their roots were kept intact; the contrary was true for plants with excised root apices. In both studied grasses, the root apoplastic barriers had an important function in the restriction of iron translocation from the root to the aerial plant parts, especially in E. crus-galli. Root apex removal negatively influenced the iron toxicity resistance mechanisms(tolerance in P. densum and avoidance in E. crus-galli).
The revegetation of mined areas poses a great challenge to the iron ore mining industry.The initial recovery process in degraded areas might rely on the use of Fe-resistant grasses.Tropical grasses, such as Paspalum densum and Echinochloa crus-galli, show different resistance strategies to iron toxicity; however, these mechanisms are poorly understood.The Fe-resistance mechanisms and direct iron toxicity as a function of root apex removal were investigated. To achieve this purpose, both grass species were grown for up to 480 hr in a nutrient solution containing 0.019 or 7 mmol/L Fe-EDTA after the root apices had been removed or maintained. Cultivation in the presence of excess iron-induced leaf bronzing and the formation of iron plaque on the root surfaces of both grass species, but was more significant on those plants whose root apex had been removed. Iron accumulation was higher in the roots, but reached phytotoxic levels in the aerial parts as well. It did not hinder the biosynthesis of chloroplastidic pigments. No significant changes in gas exchange and chlorophyll a fluorescence occurred in either grass when their roots were kept intact; the contrary was true for plants with excised root apices. In both studied grasses, the root apoplastic barriers had an important function in the restriction of iron translocation from the root to the aerial plant parts, especially in E. crus-galli. Root apex removal negatively influenced the iron toxicity resistance mechanisms(tolerance in P. densum and avoidance in E. crus-galli).
引文
Adamski,J.M.,Peters,J.A.,Danieloski,R.,Bacarin,M.A.,2011.Excess iron-induced changes in the photosynthetic characteristics of sweet potato.J.Plant Physiol.168,2056-2062.
Adamski,J.M.,Danieloski,R.,Deuner,S.,Braga,E.J.B.,de Castro,L.A.S.,Peters,J.A.,2012.Responses to excess iron in sweet potato:Impacts on growth,enzyme activities,mineral concentrations,and anatomy.Acta Physiol.Plant.34,1827-1836.
Araújo,T.O.,Freitas-Silva,L.,Santana,B.V.N.,Kuki,K.N.,Pereira,E.G.,Azevedo,A.A.,et al.,2014.Tolerance to iron accumulation and its effects on mineral composition and growth of two grass species.Environ.Sci.Pollut.R.21,2777-2784.
Barberon,M.,Vermeer,J.E.M.,De Bellis,D.,Wang,P.,Naseer,S.,Andersen,T.G.,et al.,2016.Adaptation of root function by nutrient-induced plasticity of endodermal differentiation.Cell164,447-459.
Becker,M.,Asch,F.,2005.Iron toxicity in rice-Conditions and management concepts.J.Plant Nutr.Soil Sci.168,558-573.
Bilger,W.,Bj?rkman,O.,1990.Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes,fluorescence and photosynthesis in leaves of Hedera canariensis.Photosynth.Res.25,173-185.
Briat,J.-F.,Dubos,C.,Gaymard,F.,2015.Iron nutrition,biomass production,and plant product quality.Trends Plant Sci.20,33-40.
Broadley,M.,Brown,P.,?akmak,?.,Rengel,Z.,Zhao,F.,2012.Function of Nutrients:Micronutrients.In:Marschner,P.(Ed.),Marschner's Mineral Nutrition of Higher Plants,3rd ed.Academic Press,San Diego,pp.191-248.
Celletti,S.,Paolacci,A.R.,Mimmo,T.,Pii,Y.,Cesco,S.,Ciaffi,M.,et al.,2016.The effect of excess sulfate supply on iron accumulation in three graminaceous plants at the early vegetative phase.Environ.Exp.Bot.128,31-38.
de la Fuente,C.,Pardo,T.,Alburquerque,J.A.,Martínez-Alcalá,I.,Bernal,M.P.,Clemente,R.,2014.Assessment of native shrubs for stabilisation of a trace elements-polluted soil as the final phase of a restoration process.Agric.Ecosyst.Environ.196,103-111.
Deng,D.,Wu,S.-C.,Wu,F.-Y.,Deng,H.,Wong,M.-H.,2010.Effects of root anatomy and Fe plaque on arsenic uptake by rice seedlings grown in solution culture.Environ.Pollut.158,2589-2595.
Doblas,V.G.,Geldner,N.,Barberon,M.,2017.The endodermis,a tightly controlled barrier for nutrients.Curr.Opin.Plant Biol.39,136-143.
Evert,R.F.,2006.Structure and development of the plant body-an overview.In:Evert,R.F.(Ed.),Esau's Plant Anatomy:Meristems,Cells,and Tissues of the Plant Body-their Structure,Function,and Development,3rd ed.John Wiley&Sons,Inc.,New Jersey,pp.1-13.
Genty,B.,Briantais,J.M.,Baker,N.R.,1989.The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.BBA-Gen.Subjects 990,87-92.
Halliwell,B.,1987.Oxidative damage,lipid peroxidation and antioxidant protection in chloroplasts.Chem.Phys.Lipids 44,327-340.
Hendrickson,L.,Furbank,R.T.,Chow,W.S.,2004.A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence.Photosynth.Res.82,73-81.
Hoagland,D.R.,Arnon,D.I.,1950.The Water Culture Method for Growing Plants without Soil.California Agricultural Experiment Station,Berkeley,pp.1-32.
Hodges,D.M.,Delong,J.M.,Forney,C.F.,Prange,R.K.,1999.Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Planta 207,604-611.
Huang,L.,Li,W.C.,Tam,N.F.Y.,Ye,Z.,2018.Effects of root morphology and anatomy on cadmium uptake and translocation in rice(Oryza sativa L.).J.Environ.Sci.https://doi.org/10.1016/j.jes.2018.04.005.
Jucoski,G.O.,Cambraia,J.,Ribeiro,C.,de Oliveira,J.A.,de Paula,S.O.,Oliva,M.A.,2013.Impact of iron toxicity on oxidative metabolism in young Eugenia uniflora L.plants.Acta Physiol.Plant.35,1645-1657.
Kobayashi,T.,Nishizawa,N.K.,2012.Iron uptake,translocation,and regulation in higher plants.Annu.Rev.Plant Biol.63,131-152.
Kramer,D.M.,Johnson,G.,Kiirats,O.,Edwards,G.E.,2004.New fluorescence parameters for the determination of QAredox state and excitation energy fluxes.Photosynth.Res.79,209-2018.
Li,W.C.,Deng,H.,Wong,M.H.,2017.Effects of Fe plaque and organic acids on metal uptake by wetland plants under drained and waterlogged conditions.Environ.Pollut.231,732-741.
Liu,H.,Zhang,J.,Christie,P.,Zhang,F.,2008.Influence of iron plaque on uptake and accumulation of Cd by rice(Oryza sativa L.)seedlings grown in soil.Sci.Total Environ.394,361-368.
Lobréaux,S.,Thoiron,S.,Briat,J.F.,1995.Induction of ferritin synthesis in maize leaves by an iron mediated oxidative stress.Plant J.8,443-449.
Lyubenova,L.,Pongrac,P.,Vogel-Miku?,K.,Mezek,G.K.,Vavpeti,P.,Grlj,N.,et al.,2012.Localization and quantification of Pb and nutrients in Typha latifolia by micro-PIXE.Metallomics 4,333-341.
Melis,A.,Spangfort,M.,Andersson,B.,1987.Light absorption and electron transport balance between photosystem II and photosystem I in spinach chloroplasts.Photochem.Photobiol.45,129-136.
Michalak,A.,2006.Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress.Pol.J.Environ.Stud.15,523-530.
Müller,C.,Kuki,K.N.,Pinheiro,D.T.,de Souza,L.R.,Siqueira-Silva,A.I.,Loureiro,M.E.,et al.,2015.Differential physiological responses in rice upon exposure to excess distinct iron forms.Plant Soil 391,123-138.
Müller,C.,Silveira,S.F.d.S.,Daloso,D.d.M.,Mendes,G.C.,Merchant,A.,Kuki,K.N.,et al.,2017.Ecophysiological responses to excess iron in lowland and upland rice cultivars.Chemosphere 189,123-133.
Murata,N.,Takahashi,S.,Nishiyama,Y.,Allakhverdiev,S.I.,2007.Photoinhibition of photosystem II under environmental stress.BBA-Bioenergetics 1767,414-421.
Oxborough,K.,Baker,N.R.,1997.Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qPand Fv-/Fm-;without measuring F0.Photosynth.Res.54,135-142.
Pinto,S.S.,de Souza,A.E.,Oliva,M.A.,Pereira,E.G.,2016.Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron.Sci.Agr.73,217-226.
Pugh,R.E.,Dick,D.G.,Fredeen,A.L.,2002.Heavy metal(Pb,Zn,Cd,Fe,and Cu)contents of plant foliage near the Anvil Range lead/zinc mine,Faro,Yukon Territory.Ecotox.Environ.Safe.52,273-279.
Redjala,T.,Zelko,I.,Sterckeman,T.,Legué,V.,Lux,A.,2011.Relationship between root structure and root cadmium uptake in maize.Environ.Exp.Bot.71,241-248.
Rios,C.O.,Souza,B.C.,Siqueira-Silva,A.I.,Pereira,E.G.,2017.Assessment of iron toxicity in tropical grasses with potential for revegetation of mined areas.Pol.J.Environ.Stud.26,2167-2173.
Santana,B.V.N.,de Araújo,T.O.,Andrade,G.C.,de Freitas-Silva,L.,Kuki,K.N.,Pereira,E.G.,et al.,2014.Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential.Environ.Sci.Pollut.Res.21,2550-2562.
Schmidt,W.,2006.Iron stress responses in roots of strategy Iplants.In:Barton,L.I.,Abadia,J.(Eds.),Iron Nutrition in Plants and Rhizospheric Microorganisms.Springer,Dordrecht,pp.229-250.
Sebastian,A.,Prasad,M.N.V.,2016.Iron plaque decreases cadmium accumulation in Oryza sativa L.and serves as a source of iron.Plant Biol.18,1008-1015.
Silva,J.D.O.C.,Paiva,E.A.S.,Modolo,L.V.,Nascentes,C.C.,Fran?a,M.G.C.,2013.Removal of root apices enables study of direct toxic effects of aluminum on rice(Oryza sativa L.)leaf cells.Environ.Exp.Bot.95,41-49.
Silva,L.,de Araújo,T.,Martinez,C.,de Almeida Lobo,F.,Azevedo,A.,Oliva,M.,2015.Differential responses of C3and CAM native Brazilian plant species to a SO2-and SPMFe-contaminated Restinga.Environ.Sci.Pollut.Res.22,14007-14017.
Siqueira-Silva,A.I.,Silva,L.C.,Azevedo,A.A.,Oliva,M.A.,2012.Iron plaque formation and morphoanatomy of roots from species of Restinga subjected to excess iron.Ecotox.Environ.Safe.78,265-275.
Sytar,O.,Kumar,A.,Latowski,D.,Kuczynska,P.,Strza?ka,K.,Prasad,M.N.V.,2013.Heavy metal-induced oxidative damage,defense reactions,and detoxification mechanisms in plants.Acta Physiol.Plant.35,985-999.
Tedesco,M.J.,Gianello,C.,Bissani,C.A.,Bohnen,H.,Volkweiss,S.J.,1995.Análise de solo,plantas e outros materiais.2nd ed.Universidade Federal do Rio Grande do Sul,Porto Alegre,pp.1-174.
Tylová,E.,Pecková,E.,Blascheová,Z.,Soukup,A.,2017.Casparian bands and suberin lamellae in exodermis of lateral roots:an important trait of roots system response to abiotic stress factors.Ann.Bot.120,71-85.
Velikova,V.,Yordanov,I.,Edreva,A.,2000.Oxidative stress and some antioxidant systems in acid rain-treated bean plants:protective role of exogenous polyamines.Plant Sci.151,59-66.
Wang,X.,Tam,N.F.-Y.,He,H.,Ye,Z.,2015.The role of root anatomy,organic acids and iron plaque on mercury accumulation in rice.Plant Soil 394,301-313.
Wu,L.-B.,Shhadi,M.Y.,Gregorio,G.,Matthus,E.,Becker,M.,Frei,M.,2014.Genetic and physiological analysis of tolerance to acute iron toxicity in rice.Rice 7,1-12.
Wu,L.-B.,Ueda,Y.,Lai,S.-K.,Frei,M.,2017.Shoot tolerance mechanisms to iron toxicity in rice(Oryza sativa L.).Plant Cell Environ.40,570-584.
Xu,S.,Lin,D.,Sun,H.,Yang,X.,Zhang,X.,2015.Excess iron alters the fatty acid composition of chloroplast membrane and decreases the photosynthesis rate:a study in hydroponic pea seedlings.Acta Physiol.Plant.37,1-9.
Yamaguchi,N.,Mori,S.,Baba,K.,Kaburagi-Yada,S.,Arao,T.,Kitajima,N.,et al.,2011.Cadmium distribution in the root tissues of solanaceous plants with contrasting root-to-shoot Cd translocation efficiencies.Environ.Exp.Bot.71,198-206.
Yousefi,Z.,Kolahi,M.,Majd,A.,Jonoubi,P.,2018.Effect of cadmium on morphometric traits,antioxidant enzyme activity and phytochelatin synthase gene expression(SoPCS)of Saccharum officinarum var.cp48-103 in vitro.Ecotox.Environ.Safe.157,472-481.
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Adamski,J.M.,Danieloski,R.,Deuner,S.,Braga,E.J.B.,de Castro,L.A.S.,Peters,J.A.,2012.Responses to excess iron in sweet potato:Impacts on growth,enzyme activities,mineral concentrations,and anatomy.Acta Physiol.Plant.34,1827-1836.
Araújo,T.O.,Freitas-Silva,L.,Santana,B.V.N.,Kuki,K.N.,Pereira,E.G.,Azevedo,A.A.,et al.,2014.Tolerance to iron accumulation and its effects on mineral composition and growth of two grass species.Environ.Sci.Pollut.R.21,2777-2784.
Barberon,M.,Vermeer,J.E.M.,De Bellis,D.,Wang,P.,Naseer,S.,Andersen,T.G.,et al.,2016.Adaptation of root function by nutrient-induced plasticity of endodermal differentiation.Cell164,447-459.
Becker,M.,Asch,F.,2005.Iron toxicity in rice-Conditions and management concepts.J.Plant Nutr.Soil Sci.168,558-573.
Bilger,W.,Bj?rkman,O.,1990.Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes,fluorescence and photosynthesis in leaves of Hedera canariensis.Photosynth.Res.25,173-185.
Briat,J.-F.,Dubos,C.,Gaymard,F.,2015.Iron nutrition,biomass production,and plant product quality.Trends Plant Sci.20,33-40.
Broadley,M.,Brown,P.,?akmak,?.,Rengel,Z.,Zhao,F.,2012.Function of Nutrients:Micronutrients.In:Marschner,P.(Ed.),Marschner's Mineral Nutrition of Higher Plants,3rd ed.Academic Press,San Diego,pp.191-248.
Celletti,S.,Paolacci,A.R.,Mimmo,T.,Pii,Y.,Cesco,S.,Ciaffi,M.,et al.,2016.The effect of excess sulfate supply on iron accumulation in three graminaceous plants at the early vegetative phase.Environ.Exp.Bot.128,31-38.
de la Fuente,C.,Pardo,T.,Alburquerque,J.A.,Martínez-Alcalá,I.,Bernal,M.P.,Clemente,R.,2014.Assessment of native shrubs for stabilisation of a trace elements-polluted soil as the final phase of a restoration process.Agric.Ecosyst.Environ.196,103-111.
Deng,D.,Wu,S.-C.,Wu,F.-Y.,Deng,H.,Wong,M.-H.,2010.Effects of root anatomy and Fe plaque on arsenic uptake by rice seedlings grown in solution culture.Environ.Pollut.158,2589-2595.
Doblas,V.G.,Geldner,N.,Barberon,M.,2017.The endodermis,a tightly controlled barrier for nutrients.Curr.Opin.Plant Biol.39,136-143.
Evert,R.F.,2006.Structure and development of the plant body-an overview.In:Evert,R.F.(Ed.),Esau's Plant Anatomy:Meristems,Cells,and Tissues of the Plant Body-their Structure,Function,and Development,3rd ed.John Wiley&Sons,Inc.,New Jersey,pp.1-13.
Genty,B.,Briantais,J.M.,Baker,N.R.,1989.The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.BBA-Gen.Subjects 990,87-92.
Halliwell,B.,1987.Oxidative damage,lipid peroxidation and antioxidant protection in chloroplasts.Chem.Phys.Lipids 44,327-340.
Hendrickson,L.,Furbank,R.T.,Chow,W.S.,2004.A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence.Photosynth.Res.82,73-81.
Hoagland,D.R.,Arnon,D.I.,1950.The Water Culture Method for Growing Plants without Soil.California Agricultural Experiment Station,Berkeley,pp.1-32.
Hodges,D.M.,Delong,J.M.,Forney,C.F.,Prange,R.K.,1999.Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Planta 207,604-611.
Huang,L.,Li,W.C.,Tam,N.F.Y.,Ye,Z.,2018.Effects of root morphology and anatomy on cadmium uptake and translocation in rice(Oryza sativa L.).J.Environ.Sci.https://doi.org/10.1016/j.jes.2018.04.005.
Jucoski,G.O.,Cambraia,J.,Ribeiro,C.,de Oliveira,J.A.,de Paula,S.O.,Oliva,M.A.,2013.Impact of iron toxicity on oxidative metabolism in young Eugenia uniflora L.plants.Acta Physiol.Plant.35,1645-1657.
Kobayashi,T.,Nishizawa,N.K.,2012.Iron uptake,translocation,and regulation in higher plants.Annu.Rev.Plant Biol.63,131-152.
Kramer,D.M.,Johnson,G.,Kiirats,O.,Edwards,G.E.,2004.New fluorescence parameters for the determination of QAredox state and excitation energy fluxes.Photosynth.Res.79,209-2018.
Li,W.C.,Deng,H.,Wong,M.H.,2017.Effects of Fe plaque and organic acids on metal uptake by wetland plants under drained and waterlogged conditions.Environ.Pollut.231,732-741.
Liu,H.,Zhang,J.,Christie,P.,Zhang,F.,2008.Influence of iron plaque on uptake and accumulation of Cd by rice(Oryza sativa L.)seedlings grown in soil.Sci.Total Environ.394,361-368.
Lobréaux,S.,Thoiron,S.,Briat,J.F.,1995.Induction of ferritin synthesis in maize leaves by an iron mediated oxidative stress.Plant J.8,443-449.
Lyubenova,L.,Pongrac,P.,Vogel-Miku?,K.,Mezek,G.K.,Vavpeti,P.,Grlj,N.,et al.,2012.Localization and quantification of Pb and nutrients in Typha latifolia by micro-PIXE.Metallomics 4,333-341.
Melis,A.,Spangfort,M.,Andersson,B.,1987.Light absorption and electron transport balance between photosystem II and photosystem I in spinach chloroplasts.Photochem.Photobiol.45,129-136.
Michalak,A.,2006.Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress.Pol.J.Environ.Stud.15,523-530.
Müller,C.,Kuki,K.N.,Pinheiro,D.T.,de Souza,L.R.,Siqueira-Silva,A.I.,Loureiro,M.E.,et al.,2015.Differential physiological responses in rice upon exposure to excess distinct iron forms.Plant Soil 391,123-138.
Müller,C.,Silveira,S.F.d.S.,Daloso,D.d.M.,Mendes,G.C.,Merchant,A.,Kuki,K.N.,et al.,2017.Ecophysiological responses to excess iron in lowland and upland rice cultivars.Chemosphere 189,123-133.
Murata,N.,Takahashi,S.,Nishiyama,Y.,Allakhverdiev,S.I.,2007.Photoinhibition of photosystem II under environmental stress.BBA-Bioenergetics 1767,414-421.
Oxborough,K.,Baker,N.R.,1997.Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qPand Fv-/Fm-;without measuring F0.Photosynth.Res.54,135-142.
Pinto,S.S.,de Souza,A.E.,Oliva,M.A.,Pereira,E.G.,2016.Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron.Sci.Agr.73,217-226.
Pugh,R.E.,Dick,D.G.,Fredeen,A.L.,2002.Heavy metal(Pb,Zn,Cd,Fe,and Cu)contents of plant foliage near the Anvil Range lead/zinc mine,Faro,Yukon Territory.Ecotox.Environ.Safe.52,273-279.
Redjala,T.,Zelko,I.,Sterckeman,T.,Legué,V.,Lux,A.,2011.Relationship between root structure and root cadmium uptake in maize.Environ.Exp.Bot.71,241-248.
Rios,C.O.,Souza,B.C.,Siqueira-Silva,A.I.,Pereira,E.G.,2017.Assessment of iron toxicity in tropical grasses with potential for revegetation of mined areas.Pol.J.Environ.Stud.26,2167-2173.
Santana,B.V.N.,de Araújo,T.O.,Andrade,G.C.,de Freitas-Silva,L.,Kuki,K.N.,Pereira,E.G.,et al.,2014.Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential.Environ.Sci.Pollut.Res.21,2550-2562.
Schmidt,W.,2006.Iron stress responses in roots of strategy Iplants.In:Barton,L.I.,Abadia,J.(Eds.),Iron Nutrition in Plants and Rhizospheric Microorganisms.Springer,Dordrecht,pp.229-250.
Sebastian,A.,Prasad,M.N.V.,2016.Iron plaque decreases cadmium accumulation in Oryza sativa L.and serves as a source of iron.Plant Biol.18,1008-1015.
Silva,J.D.O.C.,Paiva,E.A.S.,Modolo,L.V.,Nascentes,C.C.,Fran?a,M.G.C.,2013.Removal of root apices enables study of direct toxic effects of aluminum on rice(Oryza sativa L.)leaf cells.Environ.Exp.Bot.95,41-49.
Silva,L.,de Araújo,T.,Martinez,C.,de Almeida Lobo,F.,Azevedo,A.,Oliva,M.,2015.Differential responses of C3and CAM native Brazilian plant species to a SO2-and SPMFe-contaminated Restinga.Environ.Sci.Pollut.Res.22,14007-14017.
Siqueira-Silva,A.I.,Silva,L.C.,Azevedo,A.A.,Oliva,M.A.,2012.Iron plaque formation and morphoanatomy of roots from species of Restinga subjected to excess iron.Ecotox.Environ.Safe.78,265-275.
Sytar,O.,Kumar,A.,Latowski,D.,Kuczynska,P.,Strza?ka,K.,Prasad,M.N.V.,2013.Heavy metal-induced oxidative damage,defense reactions,and detoxification mechanisms in plants.Acta Physiol.Plant.35,985-999.
Tedesco,M.J.,Gianello,C.,Bissani,C.A.,Bohnen,H.,Volkweiss,S.J.,1995.Análise de solo,plantas e outros materiais.2nd ed.Universidade Federal do Rio Grande do Sul,Porto Alegre,pp.1-174.
Tylová,E.,Pecková,E.,Blascheová,Z.,Soukup,A.,2017.Casparian bands and suberin lamellae in exodermis of lateral roots:an important trait of roots system response to abiotic stress factors.Ann.Bot.120,71-85.
Velikova,V.,Yordanov,I.,Edreva,A.,2000.Oxidative stress and some antioxidant systems in acid rain-treated bean plants:protective role of exogenous polyamines.Plant Sci.151,59-66.
Wang,X.,Tam,N.F.-Y.,He,H.,Ye,Z.,2015.The role of root anatomy,organic acids and iron plaque on mercury accumulation in rice.Plant Soil 394,301-313.
Wu,L.-B.,Shhadi,M.Y.,Gregorio,G.,Matthus,E.,Becker,M.,Frei,M.,2014.Genetic and physiological analysis of tolerance to acute iron toxicity in rice.Rice 7,1-12.
Wu,L.-B.,Ueda,Y.,Lai,S.-K.,Frei,M.,2017.Shoot tolerance mechanisms to iron toxicity in rice(Oryza sativa L.).Plant Cell Environ.40,570-584.
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