Iron Nutrition vis-à-vis Aconitase Activity and Ferritin Accumulation in Tropical Indica Rice Cultivars Differing in Grain Iron Concentration

Binay Bhusan Panda, Srigopal Sharma, Pravat Kumar Mohapatra, Avijit Das

Division of Crop Physiology and Biochemistry, Central Rice Research Institute, Cuttack, India.
Institute of Life Sciences, Nalco Square, Bhubaneswar, India.
School of Life Sciences, Sambalpur University, Sambalpur, India.

DOI: 10.4236/ajps.2014.518299                

Abstract

Effect of Fe nutrition on Fe acquisition, aconitase enzyme activity and assimilation of the element in ferritin protein was studied in two indica rice cultivars viz. Sharbati and Lalat having contrasting grain Fe concentration. Young rice seedlings were grown in hydroponics with different levels of Fe. For comparison, the two cultivars were also grown in the field under natural conditions of rice culture. Iron accumulation, aconitase activity and ferritin level were higher in the high Fe containing cultivar, Sharbati than that in the low Fe containing cultivar, Lalat. While aconitase activity increased consistently with the increase in concentration of Fe in the growing medium, the same was not found to be true for accumulation of ferritin protein. The leaf ferritin level increased up to a certain level of Fe in the growing medium and declined thereafter. Levels of Fe in the growing medium giving maximum ferritin synthesis were found to be different in the two rice cultivars. In both cultivars, aconitase activity attained maximum level after 20 days of panicle emergence (heading). Pattern of Fe accumulation in the leaves in response to increasing Fe level in the nutrient solution paralleled with that of the aconitase activity indicating a positive correlation. It was concluded that accumulation of both ferritin protein and aconitase enzyme were influenced not only by the Fe level in the growing medium but also by the internal Fe concentration of the two cultivars.

Keywords

Rice, Iron, Aconitase, Ferritin

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Santos, L.S.D. and Oliveira, A.C.D. (2007) Rice Fe metabolism: From Source to Solution. Journal of Crop Science and Biotechnology, 10, 64-72.
[2]	Mengel, K. and Kirkby, E.A. (1982) Principles of Plant Nutrition. International Potash Institute, Bern.
[3]	Bienfait, H.F., Van Den Briel, M.L. and Mesland-Mul, N.T. (1985) Free Space Fe Pools in Roots. Generation and Mobilization. Plant Physiology, 78, 596-600. http://dx.doi.org/10.1104/pp.78.3.596
[4]	Vahl, L.C. (1991) Fe Toxicity in Rice Genotypes Irrigated by Flooding, Ph.D. Thesis, Federal University of Rio Grande do Sul, Porto Alegre.
[5]	Schmidt, W. (1999) Review Mechanisms and Regulation of Reduction-Based Fe Uptake in Plants. New Phytology, 141, 1-26. http://dx.doi.org/10.1046/j.1469-8137.1999.00331.x
[6]	Genon, J.G., Hepcee, N., Duffy, J.E., et al. (1994) Iron and Other Chemical Soil Constraints to Rice in Highland Swamps of Burundi. Plant and Soil, 166, 109-115. http://dx.doi.org/10.1007/BF02185487
[7]	CRRI Annual Report (2007) Problem Soils: Management of Iron Toxicity in Rice. India, 53.
[8]	Theil, E.C. (1987) Ferritin: Structure, Gene Regulation, and Cellular Function in Animals, Plants and Microorganisms. Annual Review of Biochemistry, 56, 289-315. http://dx.doi.org/10.1146/annurev.bi.56.070187.001445
[9]	Curie, C.G., Cassin, G., Couch, D., et al. (2009) Metal Movement within the Plant: Contribution of Nicotianamine and Yellow Stripe 1-Like Transporters. Annals of Botany, 103, 1-11. http://dx.doi.org/10.1093/aob/mcn207
[10]	Beinert, H. (2000) Fe-Sulfur Proteins: Ancient Structures, Still Full of Suppression. Biological Inorganic Chemistry, 5, 2-15. http://dx.doi.org/10.1007/s007750050002
[11]	Arnaud, N., Ravet, K., Borlotti, A., Touraine, B., Boucherez, J., Fizames, C., Briat, J.F., Cellier, F.F. and Gaymard, F. (2007) The Iron-Responsive Element (IRE)/Iron-Regulatory Protein 1 (IRP1)-Cytosolic Aconitase Iron-Regulatory Switch Does Not Operate in Plants. Biochemical Journal, 405, 523-531. http://dx.doi.org/10.1042/BJ20061874
[12]	Hentze, M.W. and Kuhn, L.C. (1996) Molecular Control of Vertebrate Iron Metabolism: mRNA-Based Regulatory Circuits Operated by Iron, Nitric Oxide, and Oxidative Stress. Proceedings of the National Academy of Sciences of the United States of America, 93, 8175-8182. http://dx.doi.org/10.1073/pnas.93.16.8175
[13]	Klausnern, R.D., Rouault, T.A. and Harford, J.B. (1993) Regulating the Fate of mRNA: The Control of Cellular Iron Metabolism. Cell, 72, 19-28. http://dx.doi.org/10.1016/0092-8674(93)90046-S
[14]	Lescure, A.M., Proudhon, D., Pesey, H., Ragland, M., Theil, E.C. and Briat, J.F. (1991) Ferritin Gene Transcription Is Regulated by Iron in Soybean Cell Cultures. Proceedings of the National Academy of Sciences of the United States of America, 88, 8222-8226. http://dx.doi.org/10.1073/pnas.88.18.8222
[15]	Jiang, T.B. (2005) Isolation and Expression Pattern Analysis of Two Ferritin Genes in Tobacco. Journal of Integrative Plant Biology, 47, 477-486. http://dx.doi.org/10.1111/j.1744-7909.2005.00044.x
[16]	Petit, J.M., van Wuytswinkel, O., Briat, J.F. and Lobréaux, S. (2001) Characterization of an Iron-Dependent Regulatory Sequence Involved in the Transcriptional Control of AtFer1 and ZmFer1 Plant Ferritin Genes by Iron. Journal of Biological Chemistry, 276, 5584-5590. http://dx.doi.org/10.1074/jbc.M005903200
[17]	da Silveira, V.C., Fadanelli, C., Sperotto, R.A., Stein, R.J., Basso, L.A., Santos, D.S., et al. (2009) Role of Ferritin in the Rice Tolerance to Iron Overload. Scientia Agricola, 66, 549-555. http://dx.doi.org/10.1590/S0103-90162009000400019
[18]	Palmer, M.J. (1964) The Relationship between Iron and the Activity of Aconitase Purified from the Leaves of Mustard (Sinapis alba). Biochemical Journal, 92, 404-410.
[19]	Panda, B.B. (2010) Biochemical Studies on Iron Metabolism in Rice Plant (Oryza sativa L.). Ph.D. Thesis, Sambalpur University, Sambalpur.
[20]	Alberts, B., John, A., Lewis, J., Raff, M., Roberst, K. and Walter, P. (2002) Molecular Biology of the Cell. 4th Edition, Garlands Science, New York.
[21]	Yoshida, S., Forno, D.A., Cock, J.H. and Gomez, K.A. (1976) Laboratory Manual for Physiological Studies of Rice. 3rd Edition, The International Rice Research Institute, Manila.
[22]	Arnon, D.I. (1949) Copper Enzymes in Isolated Chloroplasts. Polyphenol Oxidase in Beta Vulgaris. Plant Physiology, 24, 1-15. http://dx.doi.org/10.1104/pp.24.1.1
[23]	Bacon, J.S.D., Palmer, M.J. and De Kock, P.C. (1961) The Measurement of Aconitase Activity in the Leaves of Various Normal and Variegated Plants. Biochemical Journal, 78, 198-204.
[24]	Racker, E. (1950) Spectrophotometric Measurement of the Enzymatic Formation of Fumaric and Cis-Aconitic Acids. Biochimica et Biophysica Acta, 55, 270-272.
[25]	Harris, H. and Hopkinson, D.A. (1976) Handbook of Enzyme Electrophoresis in Human Genetics. North-Holland Publishing Company, Amsterdam.
[26]	Laulhere, J.P., Lescure, A.M. and Briat, J.F. (1988) Purification and Characterization of Ferritins from Maize, Pea and Soya bean Seeds. Distribution in Various Pea Organs. Journal of Biological Chemistry, 263, 10289-10294.
[27]	Chung, M.C. (1985) A Specific Iron Stain for Iron-Binding Proteins in Polyacrylamide Gels: Application to Transferrin and Lactoferrin. Analytical Biochemistry, 148, 498-502. http://dx.doi.org/10.1016/0003-2697(85)90258-1
[28]	Bradford, M.M. (1976) A Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye-Binding. Analytical Biochemistry, 72, 248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3
[29]	Stein, R.J., Ricachenevsky, F.K. and Fett, J.P. (2009) Differential Regulation of Two Rice Ferritin Genes (OsFER1 and OsFER2). Plant Science, 177, 563-569.
[30]	Becana, M., Moran, J.F. and Iturbe-Ormaetxe, I. (1988) Iron-Dependent Oxygen Free Radical Generation in Plants Subjected to Environmental Stress: Toxicity and Antioxidant Protection. Plant and Soil, 201, 137-147. http://dx.doi.org/10.1023/A:1004375732137
[31]	Tadano, T. and Yoshida, S. (1978) Chemical Changes in Submerged Soils and Their Effect on Rice Growth. In: Soils and Rice, International Rice Research Institute, Los Baños, 399-421.
[32]	Peng, X.X. and Yamauchi, M. (1993) Ethylene Production in Rice Bronzing Leaves Induced by Ferrous Iron. Plant and Soil, 149, 227-234. http://dx.doi.org/10.1007/BF00016613
[33]	Majerus, V., Bertin, P., Swenden, A., Fortemps, A., Lobréaux, S. and Lutts, S. (2007) Organ-Dependent Responses of the African Rice to Short-Term Iron Toxicity: Ferritin Regulation and Antioxidative Responses. Biologia Plantarum, 51, 303-312. http://dx.doi.org/10.1007/s10535-007-0060-6
[34]	Sahrawat, K.L., Mulbah, C.K., Diatta, S., et al. (1996) The Role of Tolerant Genotypes and Plant Nutrients in the Management of Iron Toxicity in Lowland Rice. Journal of Agricultural Science, 126, 143-149.
[35]	Machold, O. and Stephan, U.W. (1969) The Function of Iron in Porphyrin and Chlorophyll Biosynthesis. Phytochemistry, 8, 2189-2192. http://dx.doi.org/10.1016/S0031-9422(00)88179-0
[36]	Kennedy, M.C., Emptage, M.H., Dreyer, J.L. and Beinert, H. (1983) The Role of Iron in the Activation-Inactivation of Aconitase. Journal of Biological Chemistry, 258, 11098-11105.
[37]	Kennedy, M.C., Mende-Muller, L., Blondin, G.A. and Beinert, H. (1992) Purification and Characterization of Cytosolic Aconitase from Beef Liver and Its Relationship to the Fe-Responsive Element Binding Protein. Proceedings of the National Academy of Sciences of the United States of America, 89, 11730-11734. http://dx.doi.org/10.1073/pnas.89.24.11730
[38]	Peyret, P., Perez, P. and Alric, M. (1995) Structure, Genomic Organization, and Expression of the Arabidopsis Thaliana Aconitase Gene. Plant Aconitase Show Significant Homology with Mammalian Iron-Responsive Element-Binding Protein. Journal of Biological Chemistry, 270, 8131-8137. http://dx.doi.org/10.1074/jbc.270.14.8131
[39]	Branton, D. and Jacobson, L. (1962) Iron Localization in Pea Plants. Plant Physiology, 37, 546-551. http://dx.doi.org/10.1104/pp.37.4.546
[40]	Lobreaux, S., Massenet, O. and Briat, J.F. (1992) Iron Induces Ferritin Synthesis in Maize Plantlets. Plant Molecular Biology, 19, 563-575. http://dx.doi.org/10.1007/BF00026783
[41]	Murgia, I., Vazzola, V., Tarantino, D., Cellier, F., Ravet, K., Briat, J.F. and Soave, C. (2007) Knock-Out of Ferritin AtFer1 Causes Earlier Onset of Age-Dependent Leaf Senescence in Arabidopsis. Plant Physiology and Biochemistry, 45, 898-907. http://dx.doi.org/10.1016/j.plaphy.2007.09.007