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Molecular Adaptation of Peanut Metabolic Pathways to Wide Variations of Mineral Ion Composition and Concentration

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DOI: 10.4236/ajps.2012.31003    4,544 Downloads   8,239 Views   Citations

ABSTRACT

Plant evolution, nutritional genomics, and mineral nutrition have been well documented but no studies have focused on the molecular adaptation of crop metabolism to wide variations of mineral ion composition and concentration. Diversification of peanut species from primary centers of domestication in South America depended on metabolic adaptation to the mineral ion conditions of the newer habitats. Understanding the diversification molecular biology of peanut metabolic pathways will permit the synthesis of the best mineral ion combinations for doubling CO2 assimilation. Valencia and Virginia cultivars belong to different subspecies of the tetraploid Arachis hypogaea. They were planted in the absence and presence of up to 99 mM (equivalent to 166 moles per hectare) of different mineral ions. Molecular properties of the primary metabolic pathways were studied by Northern analyses using Valencia GDH-synthesized RNAs as probes for Virginia mRNA and GDH-synthesized RNAs. Messenger RNAs are silenced by homologous RNAs synthesized by GDH. Peanut cellulose was analyzed by gravimetry; and fatty acids by HPLC. Complementary DNA probes made from Valencia GDH-synthesized RNAs hybridized perfectly to Virginia mRNAs and GDH-synthesized RNAs. Wide variations in mineral ion compositions and concentrations induced the GDHs of Valencia and Virginia to synthesize RNAs that differentially down-regulated the mRNAs encoding phosphate translocator, granule-bound starch synthase, phosphoglucomutase, glucosyltransferase, acetyl CoA carboxylase, nitrate reductase, and NADH-glutamate synthase so that the percent weights of oil (41.53 ± 8.75) and cellulose (30.29 ± 3.12) were similar in the control and mineral-treated peanuts. Therefore, RNA sequences that defined the molecular adaptation of mRNAs encoding the enzymes of primary metabolism were the same in the varietal types of A. hypogaea, in agreement with genetic data suggesting that tetraploid Arachis evolved relatively recently from the wild diploid ancestral species. Another molecular adaptation was to phosphate with or without K+ ion, and it prevented the silencing by GDH-synthesized RNAs of the mRNA encoding phosphate translocator resulting to doubling of cellulosic biomass yield (41323 kg/ha) compared with the N + P + K + S-treated positive control peanut (19428 kg/ha). Molecular adaptation of primary metabolic pathways at the mRNA level to SO42- ion with or without SO42- ion did not increase cellulosic biomass yields (27057 kg/ha) compared with negative control peanut because the mRNAs encoding granule-bound starch synthase, and NADH-glutamate synthase were not silenced by GDH-synthesized RNA in the N + S, SO42-, and N + P + K + S-treated peanuts. These results could contribute towards further modeling at the mRNA level for improved mineral nutrient management of peanut production for fuel, fiber, feed, and food.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

G. Osuji, T. Brown, S. South, J. Duncan, D. Johnson and S. Hyllam, "Molecular Adaptation of Peanut Metabolic Pathways to Wide Variations of Mineral Ion Composition and Concentration," American Journal of Plant Sciences, Vol. 3 No. 1, 2012, pp. 33-50. doi: 10.4236/ajps.2012.31003.

References

[1] J. R. Harlan, J. M De Wet and E. G. Price, “Comparative Evolution of Cereals,” Evolution, Vol. 27, No. 2, 1973, pp. 311-325. doi:10.2307/2406971
[2] D. Zohary and M. Hopf, “Domestication of Plants in the Old World,” Oxford University Press, Oxford, 2000.
[3] M. E. Theodorou and W. C. Plaxton, “Metabolic Adaptations of Plant Respiration to Nutritional Phosphate Deprivation,” Plant Physiology, Vol. 101, No. 2, 1993, pp. 339-344.
[4] H. J. Bohnert and E. Sheveleva, “Plant Stress Adaptation: Making Metabolism Move,” Current Opinion in Plant Biology, Vol. 1, No. 3, 1998, pp. 267-274. doi:10.1016/S1369-5266(98)80115-5
[5] M. D. Purugganan and D. Q. Fuller, “The Nature of Selection during Plant Domestication,” Nature, Vol. 457, 2009, pp. 843-848. doi:10.1038/nature07895
[6] R. L. Meyer and N. Rask, “Major Food and Energy Crops: Trends and Prospects,” In: P. V. Ammirato, D. A. Evans, W. R. Sharp and Y. Yamada, Eds., Handbook of Plant Cell Culture Crop Species, Macmillan, New York, Vol. 2, 1984, pp. 19-47.
[7] A. Krapovickas, “Evolution of the Genus Arachis,” In: R. Moav, Ed., Agricultural Genetics, Wiley, New York, 1973, pp. 135-151.
[8] W. C. Gregory and M. P. Gregory, “Groundnut,” In: N. W. Simmonds, Ed., Evolution of Crop Plants, Longman, London and New York, 1976, pp. 151-154.
[9] B. Jayashree, F. Morgan, I. Dan, D. Jeff and H. C. Jonathan, “Analysis of Genomic Sequences from Peanut,” Electronic Journal of Biotechnology, Vol. 8, No. 3, 2005, pp. 226-237.
[10] Y. P. S. Bajaj, “Peanut,” In: P. V. Ammirato, D. A. Evans, W. R. Sharp and Y. Yamada, Eds., Handbook of Plant Cell Culture Crop Species, Macmillan, New York, Vol. 13, 1984, pp. 193-326.
[11] Z. Rengel, “Mineral Nutrition of Crops,” Food Products Press, New York, London, Oxford, 1999.
[12] J. F. Doebley, B. S. Gaunt and B. D. Smith, “The Molecular Genetics of Crop Domestication,” Cell, Vol. 127, No. 7, 2006, pp. 1309-1329. doi:10.1016/j.cell.2006.12.006
[13] M. R. Broadley and P. J. White, “Plant Nutritional Genomics,” Blackwell Publishing and CRC Press, Oxford, 2005.
[14] C. Colijn, A. Brandes, J. Zucker, D. S. Lun, B. Weiner, M. R. Farhat, T. Chen, D. B. Moody, M. Murray and J. E. Galagan, “Interpreting Expression Data with Metabolic Flux Models: Predicting Mycobacterium Tuberculosis Mycolic Acid Production,” PLoS Computational Biology, Vol. 5, No. 8, 2009, e1000489 doi:10.1371/journal.pcbi.1000489
[15] J. Hay and J. Schwender, “Computational Analysis of Storage Synthesis in Developing Brassica Napus L. (OilSeed Rape) Embryos: Flux Variability Analysis in Relation to 13C Metabolic Flux Analysis,” The Plant Journal, Vol. 67, No. 3, 2011, pp. 513-525. doi:10.1111/j.1365-313X.2011.04611.x
[16] J. A. Morgan and D. Rhodes, “Mathematical Modeling of Plant Metabolic Pathways,” Metabolic Engineering, Vol. 4, No. 1, 2002, pp. 80-89. doi:10.1006/mben.2001.0211
[17] G. O. Osuji and W. C. Madu, “Ammonium Ion-Dependent Isomerization of Glutamate Dehydrogenase in Relation to Glutamate Synthesis in Maize,” Phytochemistry, Vol. 39, No. 3, 1995, pp. 495-503. doi:10.1016/0031-9422(94)00976-Z
[18] G. O. Osuji and W. C. Madu, “Regulation of Peanut Glutamate Dehydrogenase by Methionine Sulphoximine,” Phytochemistry, Vol. 46, No. 5, 1997, pp. 817-825. doi:10.1016/S0031-9422(97)00395-6
[19] G. O. Osuji, A. S. Mangaroo, J. Reyes, A. Bulgin and V. Wright, “Biomass Enhancement in Maize and Soybean in Response to Glutamate Dehydrogenase Isomerization,” Biologia Plantarum, Vol. 47, 2003, pp. 45-52. doi:10.1023/A:1027324713682
[20] G. O. Osuji, T. K. Brown, S. M. South, J. C. Duncan and D. Johnson, “Doubling of Crop Yield Through Permutation of Metabolic Pathways,” Advances in Biosciences and Biotechnology, Vol. 2, No. 5, 2011, pp. 364-379. doi:10.4236/abb.2011.25054
[21] G. O. Osuji, T. K. Brown and S. M. South, “Optimized Fat and Cellulosic Biomass Accumulation in Peanut Through Biotechnology,” International Journal Biotechnology & Biochemistry, Vol. 6, 2010, pp. 455-476.
[22] A. J. Norden, O. D. Smith and D. W. Gorbet, “Breeding of the Cultivated Peanut,” In: H. E. Pattee and C. T. Young, Eds., Peanut Science and Technology, American Peanut Research and Education Society, Inc., Yoakum, 1982, pp. 95-123.
[23] G. O. Osuji, J. Konan and G. M’Mbijjewe, “RNA Synthetic Activity of Glutamate Dehydrogenase,” Applied Biochemistry and Biotechnology, Vol. 119, No. 3, 2004, pp. 209-228. doi:10.1007/s12010-004-0003-z
[24] D. Grierson, A. Slater, J. Speirs and G. A. Tucker, “The Appearance of Polygalacturonase mRNA in Tomatoes,” Planta, Vol. 163, No. 2, 1985, pp. 263-271. doi:10.1007/BF00393517
[25] G. O. Osuji, T. K. Brown and S. M. South, “Nucleotide-Dependent Reprogramming of mRNAs Encoding Acetyl Coenzyme A Carboxylase and Lipoxygenase in Relation to the Fat Contents of Peanut,” Journal of Botany, 2009. doi:10.1155/2009/278324
[26] G. O. Osuji and T. Brown, “Environment-Wide Reprogramming of mRNAs Encoding Phosphate Translocator and Glucosyltransferase in Relation to Cellulosic Biomass Accumulation in Peanut,” The ICFAI Journal Biotechnology, Vol. 1, No. 4, 2007, pp. 35-47.
[27] G. O. Osuji, A. S. Mangaroo and P. S. Roberts, “In Vitro Isomerization of Glutamate Dehydrogenase in Relation to Phytosequestration of Lead,” SAAS Bulletin, Biochemistry and Biotechnology, Vol. 14, 2001, pp. 60-72.
[28] D. Cammaerts and M. Jacobs, “A Study of the Polymorphism and the Genetic Control of the Glutamate Dehydrogenase Isoenzymes in Arabidopsis thaliana,” Plant Science Letters, Vol. 31, No. 1, 1983, pp. 67-73. doi:10.1016/0304-4211(83)90130-X
[29] G. Osuji, T. K. Brown and S. M. South, “Discovery of RNA Synthetic Activity of Glutamate Dehydrogenase and its Application in Drug Metabolism Research,” The Open Drug Metabolism Journal, Vol. 2, 2008, pp. 1-13. doi:10.2174/1874073100802010001
[30] S. Knappe, U. Flugge and K. Fischer, “Analysis of the Plastidic Phosphate Translocator Gene Family in Arabidopsis and Identification of New Phosphate Translocator-Homologous Transporters, Classified by their Putative Substrate-Binding Site,” Plant Physiology, Vol. 131, No. 3, 2003, pp. 1178-1190. doi:10.1104/pp.016519
[31] M. G. James, K. Denyer and A. M. Myers, “Starch Synthesis in the Cereal Endosperm,” Current Opinion in Plant Biology, Vol. 6, No. 3, 2003, pp. 215-222. doi:10.1016/S1369-5266(03)00042-6
[32] E. J. Davis, I. J. Tetlow, C. G. Bowsher and M. J. Emes, “Molecular and Biochemical Characterization of Cytosolic Phosphoglucomutase in Wheat Endosperm,” Journal Experimental Botany, Vol. 54, No. 386, 2003, pp. 1351-1360. doi:10.1093/jxb/erg151
[33] M. Swissa, Y. Aloni, H. Weinhouse and M. Benizman, “Intermediary Steps in Acetobacter Xylinum Cellulose Synthesis: Studies with Whole Cells and Cell-Free Preparations of the Wild Type and Celluloseless Mutant,” Journal of Bacteriology, Vol. 143, 1980, pp. 1142-1150.
[34] L. Peng, K. Yasushi, H. Pat and D. Deborah, “Sitosterol-β-Gluciside as Primer for Cellulose Synthesis in Plants,” Science, Vol. 295, No. 5552, 2002, pp. 147-150. doi:10.1126/science.1064281
[35] I. M. Saxena and R. M. Brown, “Identification of Cellulose Synthase(s) in Higher Plants: Sequence Analysis of Processive β-Glycosyltransferases With the Common Motif ‘D, D, D35Q(R,Q)XRW’,’’ Cellulose, Vol. 4, No. 1, 1977, pp. 33-49. doi:10.1023/A:1018411101036
[36] W. B. Parker, L. C. Marshall, J. D. Burton, D. A. Somers, D. L. Wyse, J. W. Gronwald and B. G. Gengenbach, “Dominant Mutations Causing Alterations in Acetyl-Coenzyme a Carboxylase Confer Tolerance to Cyclohexanedione and Aryloxyphenoxypropionate Herbicides in Maize,” Proceedings National Academy Science, Vol. 87, No. 18, 1990, pp. 7175-7179. doi:10.1073/pnas.87.18.7175
[37] P. M. C. Smith and C. A. Atkins, “Purine Biosynthesis: Big in Cell Division, Even Bigger in Nitrogen Assimilation,” Plant Physiology, Vol. 128, No. 3, 2002, pp. 793-802. doi:10.1104/pp.010912
[38] K. M. Schnorr, P. Nygaard and M. Laloue, “Molecular Characterization of Arabidopsis thaliana cDNAs Encoding three Purine Biosynthetic Enzymes,” The Plant Journal, Vol. 6, No. 1, 1999, pp. 113-121. doi:10.1046/j.1365-313X.1994.6010113.x
[39] A. Kleinhofs, R. L. Warner, J. M. Lawrence, J. M. Melzer and D. A. Kudrna, “Molecular Genetics of Nitrate Reductase in Barley,” In: J. L. Wray and J. R. Kinghorn, Eds., Molecular and Genetic Aspects of Nitrate Assimilation, Oxford Science Publications, Oxford, 1989, pp. 197-211.
[40] C. P. Vance, S. S. Miller, R. G. Gregerson, D. A. Samac, D. L. Robinson and J. S. Gantt, “Alfalfa NADH-Dependent Glutamate Synthase: Structure of the Gene and Importance in Symbiotic N2 Fixation,” Plant Journal, Vol. 8, No. 3, 1995, pp. 345-358. doi:10.1046/j.1365-313X.1995.08030345.x
[41] L. Husted,” Cytological Studies on the Peanut, Arachis II Chromosome Number, Morphology and Behavior and Their Application to the Origin of Cultivated Forms,” Cytologia, Vol. 7, No. 3, 1936, pp. 396-423. doi:10.1508/cytologia.7.396
[42] U. Klahre, S. A. Leuenberger, V. A. Iglesias and F. Meins, “High Molecular Weight RNAs and Small Interfering RNAs Induce Posttranscriptional Gene Silencing in Plants,” Proceedings of the National Academy of Sciences of the USA, Vol. 10, 2002, pp. 1973-1078.
[43] C. A. Perez-Novo, C. Claeys, F. Speleman, P. V. Cauwenberge, C. Bachert and J. Vandesompele, “Impact of RNA Stability on Reference Gene Expression Stability,” Biotechniques, Vol. 39, No. 1, 2005, pp. 52-56. doi:10.2144/05391BM05
[44] D. Q. Fuller, “Contrasting Patterns in Crop Domestication and Domestication Rates: Recent Archaeobotanical Insights from the Old World,” Annals of Botany (London), Vol. 100, No. 51, 2007, pp. 903-924. doi:10.1093/aob/mcm048
[45] K. O. Burkey, F. L. Booker W. A. Pursley and A. S. Heagle, “Elevated Carbon Dioxide and Ozone Effects on Peanut: II. Seed Yield and Quality,” Crop Science, Vol. 47, No. 4, 2007, pp. 1488-1497. doi:10.2135/cropsci2006.08.0538
[46] P. Horton, “Prospects for Crop Improvement Through the Genetic Manipulation of Photosynthesis: Morphological and Biochemical Aspects of Light Capture,” Journal of Experimental Botany, Vol. 51, No. 1, 2000, pp. 475-485. doi:10.1093/jexbot/51.suppl_1.475
[47] R. A. Richards, “Selectable Traits to Increase Crop Photosynthesis and Yield of Grain,” Journal of Experimental Botany, Vol. 51, No. 1, 2000, pp. 447-458. doi:10.1093/jexbot/51.suppl_1.447

  
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