Abstract
Iron toxicity is a major nutritional disorder in irrigated and rainfed waterlogged rice. To elucidate mechanisms involved in tolerance to iron toxicity, plants from one cultivar susceptible to iron toxicity (BR-IRGA 409) and two tolerant cultivars (EPAGRI 108 and EPAGRI 109) were grown in the field, at an iron-toxic site and at a control site in Southern Brazil. We evaluated chlorophyll concentrations, carbonyl concentrations, iron concentrations in leaves and roots, antioxidative enzyme activities (SOD, APX, CAT, GR and DHR), concentrations of reduced and oxidized forms of ascorbate and glutathione, and gene expression profile of four SOD genes in rice leaves. Only plants from the susceptible cultivar showed symptoms of iron toxicity when grown at the iron-toxic site, accumulating high levels of iron in leaves. EPAGRI 108 plants had the lowest iron concentration in leaves and reached the highest iron concentration in the root symplast, suggesting that the capacity to safely store iron in root cells and to limit iron translocation to shoots could be a tolerance mechanism in this cultivar. Plants from the susceptible cultivar showed higher APX activity as well as higher DHA and GSSG concentrations. Plants from the EPAGRI 109 cultivar accumulated high iron levels in leaves, and showed the highest SOD, GR and DHR activities when grown in the iron-toxic site. The same cultivar also showed the highest expression of three out of four SOD genes tested. Therefore, the two tolerant cultivars seem to rely on different mechanisms to deal with iron toxicity in field conditions: limiting iron translocation to the shoot or inducing enzymes-dependent leaf tolerance.
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Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
Ando T, Yoshida S, Nishiyama I (1983) Nature of oxidizing power of rice roots. Plant Soil 72:57–71
Audebert A, Sahrawat KL (2000) Mechanisms for iron toxicity tolerance in lowland rice. J Plant Nutr 23:1877–1885
Bacha RE, Ishiy T (1986) Toxicidad por hierro em arroz: metodologia para seleccionar genótipos resistentes en Brasil. Bol Prog CIAT 7:1–4
Becker M, Asch F (2005) Iron toxicity - conditions and management concepts. J Plant Nutr Soil Sci 168:558–573
Benckiser G, Santiago S, Neue HU, Watanabe I, Ottow JCG (1984) Effect of iron fertilization on exudation, dehydrogenase activity, iron-reducing populations and Fe++ formation in the rhizosphere of rice (Oryza sativa L.) in relation to iron toxicity. Plant Soil 79:305–316
Beyer WF, Fridovich I (1987) Assaying of superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Bowler C, van Camp W, van Montagu M, Inzé D (1994) Superoxide dismutases in plants. Crit Rev Plant Sci 13:199–218
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Counce PA, Keisling TC, Mitchell AJ (2000) A Uniform, objective, and adaptive system for expressing rice development. Crop Sci 40:436–443
Fageria NK, Rabelo NA (1987) Tolerance of rice cultivars to iron toxicity. J Plant Nutr 10:653–661
Fang WC, Wang JW, Lin CC, Kao CH (2001) Iron induction of lipid peroxidation and effects on antioxidative enzyme activities in rice leaves. Plant Growth Regul 35:75–80
Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159
Green MS, Etherington JR (1977) Oxidation of ferrous iron by rice (Oryza sativa L.) roots: a mechanism for waterlogging tolerance. J Exp Bot 28:678–690
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212
Kato Y, Urano J, Maki Y, Ushimaru T (1997) Purification and characterization of dehydroascorbate reductase from rice. Plant Cell Physiol 38:173–178
Kim D, Shibato J, Agrawal GK, Fujihara S, Iwahashi H, Kim DH, Shim I, Rakwal R (2007) Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol Cell 24:45–59
Klapheck S, Zimmer Z, Cosse H (1990) Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant Cell Physiol 31:1005–1013
Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638
Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A, Ahn B, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Method Enzymol 186:464–478
McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of trangenic Alfafa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181
Mhamdi A, Noctor G, Baker A (2012) Plant catalases: peroxisomal redox guardians. Arch Biochem Biophys 525:181–194
Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family in rice. Plant Physiol 138:1903–1913
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Mol Biol 49:249–279
Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850
Okamura M (1980) An improved method for the determination of L-ascorbic acid and L-dehydroascorbic acid in blood plasma. Clin Chim Acta 103:259–268
Olaleye AO, Tabi FO, Ogunkule AO, Singh BN, Sahrawat KL (2001) Effect of toxic iron concentration on the growth of lowland rice. J Plant Nutr 24:441–457
Ottow JCG, Benckiser GH, Watanabe IJ, Santiago S (1982) A multiple nutritional soil stress as the prerequisite for iron toxicity of wetland rice (Oryza sativa L.). Trop Agr 60:102–106
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Pereira EG, Oliva MA, 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 201:81–92
Ponnamperuma FN (1972) The chemistry of submerged soils. Adv Agron 24:29–96
Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, Lutts S, Lefèvre I (2012) Combined transcriptomic and physiological approaches reveal strong differences between short- and long-term response of rice (Oryza sativa) to iron toxicity. Plant Cell Environ 35:1837–1859
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Ricachenevsky FK, Sperotto RA, Menguer PK, Fett JP (2010) Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence. Mol Biol Rep 37:3735–3745
Ross CW (1974) Plant physiology laboratory manual. Wadsworth Publishing Company, Belmont
Sahrawat KL (2000) Elemental composition of rice plants as affected by iron toxicity under field conditions. Comm Soil Sci Plant Anal 31:2819–2827
Sahrawat KL (2004) Iron toxicity in wetland rice and the role of other nutrients. J Plant Nutr 27:1471–1504
Sahrawat KL, Mulbah CK, Diatta K, Delaune RD, Patrick WH, Singh BN, Jones MP (1996) The role of tolerant genotypes and plant nutrients in the management of iron toxicity in lowland rice. J Agr Sci 126:143–149
Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochem 33:561–565
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
Silveira VC, Oliveira AP, Sperotto RA, Espindola LS, Amaral L, Dias JF, Cunha JB, Fett JP (2007) Influence of iron on mineral status of two rice (Oryza sativa L.) cultivars. Braz J Plant Physiol 12:127–139
Stein RJ, Duarte GL, Spohr MG, Lopes SIG, Fett JP (2009) Distinct physiological responses of two rice cultivars subjected to iron toxicity in the field. Ann Appl Biol 154:269–277
Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Kishitani S, Takabe T, Yokota S, Takabe T (1999) Salt tolerance of transgenic rice overexpressing yeast mitochondrial Mn-SOD in chloroplasts. Plant Sci 148:131–138
Taylor G, 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
Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677
Winslow MD, Yamauchi M, Alluri K, Masajo TM (1989) Reducing iron toxicity in rice with resistant genotype and ridge planting. Agron J 81:458–460
Wu P, Hu B, Liao CY, Zhu JM, Wu YR, Senadhira D, Paterson AH (1998) Characterization of tissue tolerance to iron by molecular markers in different lines of rice. Plant Soil 203:217–226
Yamauchi M, Peng XX (1995) Iron toxicity and stress-induced ethylene production in rice leaves. Plant Soil 173:21–28
Acknowledgments
This work was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brazil), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil) and FAPERGS (Fundação de Apoio à Pesquisa do Estado do Rio Grande do Sul—Brazil).
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Stein, R.J., Lopes, S.I.G. & Fett, J.P. Iron toxicity in field-cultivated rice: contrasting tolerance mechanisms in distinct cultivars. Theor. Exp. Plant Physiol. 26, 135–146 (2014). https://doi.org/10.1007/s40626-014-0013-3
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DOI: https://doi.org/10.1007/s40626-014-0013-3