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 AS  Vol.8 No.10 , October 2017
Horticultural Production of Ultra High Resveratrol Peanut
Abstract:
Background: Resveratrol naturally occurring antioxidant in peanut (Legume: Arachis hypogaea) has phytochemical human health dietary effects associated with reduced inflammatory cancer risks. Its levels in peanut are ultra-low and variable (0 to 26 μg·g-1), which has made it difficult to market as a consistent high resveratrol produce. Objective: Understanding the regulation of resveratrol accumulation in peanut might lead to development of new techniques for optimizing and stabilizing its yield. Method: Peanuts were cultivated in horticultural field plots and treated with solutions of mineral salts (sulfate, potassium, phosphate, ammonium ion) that were optimized in stoichiometric (reactive) ratios. Peanut seed’s RNAs were subjected to Northern blot analysis for profiling the RNAs synthesized by glutamate dehydrogenase (GDH), and mRNAs encoding resveratrol synthase. The seed’s extracts were analyzed by GC-MS for determination of the resveratrol and fatty acid compositions. Result: Stoichiometric mixes of mineral ions induced the peanut GDH to synthesize some RNA that silenced the mRNAs encoding resveratrol synthase, phosphoglucomutase, isocitrate lyase, malate synthase, enolase, phosphoenolpyruvate carboxylase, malate dehydrogenase, and phosphoglycerate mutase in the control, KN-, and NPKS-treated but not in the NPPK-treated peanut. These resulted to decreased resveratrol content (6.0 μg·g-1) in the control peanut but maximized it (1.15 mg·g-1) in the NPPK-treated peanut. Therefore, resveratrol accumulation was optimized by coupling of glycolysis and citric-glyoxylic acid cycles to resveratrol biosynthesis. Fatty acid content of control (55.6 g·kg-1) was higher than the NPKS-treated (48.5 g·kg-1) and NPPK-treated peanut (44.9 g·kg-1) meaning that malonyl-CoA intermediate in both fatty acid and stilbenoid pathways was diverted to support maximum resveratrol biosynthesis in the NPPK-treated peanut. Conclusion: The functional coupling of citric-glyoxylic acid cycles and glycolysis to optimize resveratrol biosynthesis may encourage development of horticultural technology specific for production of ultra-high resveratrol peanuts.
Cite this paper: Osuji, G. , Johnson, P. , Duffus, E. , Woldesenbet, S. and Kirven, J. (2017) Horticultural Production of Ultra High Resveratrol Peanut. Agricultural Sciences, 8, 1173-1194. doi: 10.4236/as.2017.810086.
References

[1]   Sanders, T.H., McMichael, R.W. and Hendrix, K.W. (2000) Occurrence of Resveratrol in Edible Peanuts. Journal of Agricultural and Food Chemistry, 48, 1243-1246.
https://doi.org/10.1021/jf990737b

[2]   Creasy, L.L. and Coffee, M. (1988) Phytoalexin Production Potential of Grape Berries. Journal of the American Society for Horticultural Science, 113, 230-234.

[3]   Schroder, G., Brown, J.W. and Schroder, J. (1998) Molecular Analysis of Resveratrol Synthase cDNA, Genomic Clones and Relationship with Chalcone Synthase. European Journal of Biochemistry, 172, 161-169.
https://doi.org/10.1111/j.1432-1033.1988.tb13868.x

[4]   Giovinazzo, G., Ingrosso, I., Paradiso, A., De Gara, L. and Santino, A. (2012) Resveratrol Biosynthesis: Plant Metabolic Engineering for Nutritional Improvement of Food. Plant Foods for Human Nutrition, 67, 191-199.
https://doi.org/10.1007/s11130-012-0299-8

[5]   Jang, M., Cai, G.O., Udeani, K.V., Slowing, C.F., et al. (1997) Cancer Chemopreventive Activity of Resveratrol, a Natural Product Derived from Grapes. Science, 275, 218-220.
https://doi.org/10.1126/science.275.5297.218

[6]   Wu, J.M., Wang, Z.R., Hsieh, T.C., Bruder, J.L., et al. (2001) Mechanism of Cardioprotection by Resveratrol, a Phenolic Antioxidant Present in Red Wine. International Journal of Molecular Medicine, 8, 3-17.

[7]   Nolan, C.J., Damm, P. and Prentki, M. (2011) Type 2 Diabetes across Generations: From Pathophysiology to Prevention and Management. The Lancet, 378, 169-181.

[8]   Beak, S.-H., Shin, W.-C., Ryu, H.-S., Lee, D.-W., Moon, E., et al. (2013) Creation of Resveratrol-Enriched Rice for the Treatment of Metabolic Syndrome and Related Diseases. PLoS ONE, 8, e57930.
https://doi.org/10.1371/journal.pone.0057930

[9]   Guarente, L. (2006) Sirtuins as Potential Targets for Metabolic Syndrome. Nature, 444, 868-874.
https://doi.org/10.1038/nature05486

[10]   Szajdek, A. and Borowska, E.J. (2009) Bioactive Compounds and Health-Promoting Properties of Berry Fruits: A Review. Plant Foods for Human Nutrition, 63, 147-156.
https://doi.org/10.1007/s11130-008-0097-5

[11]   Rimando, A.M., Nagmani, R., Feller, D.R. and Yokoyama, W. (2005) Pterostilbene, a New Argonist for the Peroxizome Proliferator-Activated Receptor α-Isoform, Lowers Plasma Lipoproteins and Cholesterol in Hypercholoesteromic Hamsters. Journal of Agricultural and Food Chemistry, 53, 3403-3407.
https://doi.org/10.1021/jf0580364

[12]   McCormack, D. and McFadden, D. (2013) A Review of Pterostilbene Antioxidant Activity and Disease Modification. Oxidative Medicine and Cell Longevity.
https://doi.org/10.1155/2013/575482

[13]   Wang, L., Heredia, A., Song, H., Zhang, Z., et al. (2004) Resveratrol Glucuronides as the Metabolites of Resveratrol in Humans: Characterization, Synthesis, and Anti-HIV Activity. Journal of Pharmaceutical Sciences, 93, 2448-2454.
https://doi.org/10.1002/jps.20156

[14]   Jungong, C.S. and Novikov, A.V. (2012) Practical Preparation of Resveratrol 3-O-β-D-Glucuronide. Synthetic Communications: An International Journal for Rapid Communication of Synthetic Organic Chemistry, 42, 3589-3597.
https://doi.org/10.1080/00397911.2011.585733

[15]   McMurtrey, K.D., Minn, J., Pobanz, K. and Schultz, T.P. (1994) Analysis of Wines for Resveratrol using Direct Injection High-Pressure Liquid Chromatography with Electrochemical Detection. Journal of Agricultural and Food Chemistry, 42, 1997-2000.
https://doi.org/10.1021/jf00046a001

[16]   Bioscience Technology (2014) Red Wine May Not Prevent Heart Disease, Prolong Life.
http://www.biosciencetechnology.com

[17]   Wang, K.H., Lai, Y.H., Chang, J.C., et al. (2005) Germination of Peanut Kernels to Enhance Resveratrol Biosynthesis and Prepare Sprouts as a Functional Vegetable. Journal of Agricultural and Food Chemistry, 53, 242-246.

[18]   Chung, I., Park, M.R., Chun, J.C. and Yun, S.J. (2003) Resveratrol Accumulation and Resveratrol Synthase Gene Expression in Response to Abiotic Stress and Hormones in Peanut Plants. Plant Science, 164, 103-109.

[19]   Sobolev, V.S. and Cole, R.J. (1999) Trans-Resveratrol Content in Commercial Peanuts and Peanut Products. Journal of Agricultural and Food Chemistry, 47, 1435-1439.
https://doi.org/10.1021/jf9809885

[20]   Fletcher, S.M. (2009) Evaluation and Results Report on the National Peanut Board’s Domestic Peanut Market Program 1st quarter 2005-3rd quarter 2009.

[21]   Aleynova, O.A., Dubrovina, A.S., Manyakhin, A.Y., Keratin, Y.A. and Kiselev, K.V. (2015) Regulation of Resveratrol Production in Vitis amurensis Cell Cultures by Calcium-Dependent Protein Kinases. Applied Biochemistry and Biotechnology, 175, 1460-1476.
https://doi.org/10.1007/s12010-014-1384-2

[22]   Resurreccion, V., Anna, A., Rudolf, J.L., Phillips, R.D. and Chinnan, M. (2005) Method for Enhancing Content of Peanut Compositions (Patent No. US 766455).

[23]   Fritzemeier, K.H., Rofls, C.H., Pfau, J. and Kindl, H. (1983) Action of Ultraviolet-C on Stilbene Formation in Callus of Arachis hypogaea. Planta, 159, 25-29.
https://doi.org/10.1007/BF00998810

[24]   Paiva, N.L. and Hipskind, J.D. (2005) Transgenic Legume Plants Modified to Produce Resveratrol Glucoside and Uses Thereof. US Patent 6974895.

[25]   Farina, A., Ferranti, C. and Marra, C. (2006) An Improved Synthesis of Resveratrol. Natural Product Research, 20, 247-252.
https://doi.org/10.1080/14786410500059532

[26]   Trants, E., Panopoulos, N. and Ververidis, F. (2009) Metabolic Engineering of the Complete Pathway Leading to Heterologous Biosynthesis of Various Flavonoids and Stilbenoids in Saccharomyces cerevisiae. Metabolic Engineering, 11, 355-366.

[27]   Wang, H., Liu, L., Guo, Y.X., et al. (2007) Biotransformation of Piceid in Polygonum cuspidatum to Resveratrol by Aspergillus oryzea. Applied Microbiology and Biotechnology, 75, 763-768.

[28]   Hasan, M.M., Cha, M., Bajpai, V.K. and Baek, K. (2013) Production of a Major Stilbene Phytoalexin, Resveratrol in Peanut (Arachis hypogaea) and Peanut Products: A Mini Review. Reviews in Environmental Science and Biotechnology, 12, 209-221.
https://doi.org/10.1007/s11157-012-9294-7

[29]   Yu, O. and Jez, J. (2008) Nature’s Assembly Line: Biosynthesis of Simple Phenylpropanoids and Polyketides. The Plant Journal, 54, 750-763.
https://doi.org/10.1111/j.1365-313X.2008.03436.x

[30]   Osuji, G.O., Duffus, E., Johnson, P., Woldesenbet, S., Weerasooriya, A., Ampim, P.A., Carson, L., Jung, Y., South, S., Idan, E., Johnson, D., Clarke, D., Lawton, B., Parks, A., Fares, A. and Johnson, A. (2015) Enhancement of the Essential Amino Acid Composition of Food Crop Proteins through Biotechnology. American Journal Plant Sciences, 6, 3091-3108.
https://doi.org/10.4236/ajps.2015.619302

[31]   Jeandet, P., Bessis, R., Adrian, M., Yvin, J. and Joubert, J. (2000) Use of Aluminum Chloride as a Resveratrol Synthesis Elicitor. US Patent Number US6080701A.
http://www.google.com/patents/US6080701

[32]   Kiselev, K.V., Shumakova, O.A. and Manyakhin, A.Y. (2013) Effect of Plant Stilbene Precursors on the Biosynthesis of Resveratrol in Vitis amurensis Rupr. Cell Cultures. Applied Biochemistry and Microbiology, 49, 53-58.
https://doi.org/10.1134/S0003683813010079

[33]   Rietra, R.P.J.J., Heinen, M., Dimkpa, C. and Bindraban, P.S. (2015) Effects of Nutrient Antagonism and Synergism on Fertilizer Use Efficiency. VFRC Report 2015/5. Virtual Fertilizer Research Center, Washington DC, 42 p.

[34]   Osuji, G.O., Brown, T.K., South, S.M., Johnson, D. and Hyllam, S. (2012) Molecular Modeling of Metabolism for Allergen-Free Low Linoleic Acid Peanuts. Applied Biochemistry and Biotechnology, 168, 805-823.
https://doi.org/10.1007/s12010-012-9821-6

[35]   Osuji, G.O., Brown, T.K., South, S.M., Duncan, J.C. and Johnson, D. (2011) Doubling of Crop Yield through Permutation of Metabolic Pathways. Advances in Bioscience and Biotechnology, 2, 364-379.
https://doi.org/10.4236/abb.2011.25054

[36]   Osuji, G.O., Brown, T.K. and South, S.M. (2010) Optimized Fat and Cellulosic Biomass Accumulation in Peanut through Biotechnology. International Journal of Biotechnology & Biochemistry, 6, 451-472.

[37]   Osuji, G.O., Konan, J. and M’Mbijjewe, G. (2004) RNA Synthetic Activity of Glutamate Dehydrogenase. Applied Biochemistry and Biotechnology, 119, 209-228.
https://doi.org/10.1007/s12010-004-0003-z

[38]   Osuji, G.O., Reyes, J.C. and Mangaroo, A.S. (1998) Glutamate Dehydrogenase Isomerization: A Simple Method for Diagnosing Nitrogen, Phosphorus, and Potassium Sufficiency in Maize (Zea mays L.). Journal of Agricultural and Food Chemistry, 46, 2395-2401.
https://doi.org/10.1021/jf971065x

[39]   Osuji, G.O., Mangaroo, A.S., Reyes, J. and Wright, V. (2003) Biomass Enhancement in Maize and Soybean in Response to Glutamate Dehydrogenase Isomerization. Biologia Plantarum, 47, 45-52.

[40]   Osuji, G.O., Brown, T.K. and South, S.M. (2008) Discovery of the RNA Synthetic Activity of GDH and Its Application in Drug Metabolism Research. The Open Drug Metabolism Journal, 2, 1-13.
https://doi.org/10.2174/1874073100802010001

[41]   Osuji, G.O., Brown, T.K. and South, S.M. (2009) Nucleotide-Dependent Reprogramming of mRNAs Encoding Acetyl Coenzyme a Carboxylase and Lipoxygenase in Relation to the Fat Contents of Peanut. Journal of Botany, 2009, Article ID: 278324.
https://doi.org/10.1155/2009/278324

[42]   Osuji, G.O. and Brown, T. (2007) Environment-Wide Reprogramming of mRNAs Encoding Phosphate Translocator and Glucosyltransferase in Relation to Cellulosic Biomass Accumulation in Peanut. ICFAI Journal of Biotechnology, 1, 35-47.

[43]   Streb, S., Elgi, B., Eicke, S. and Zeeman, S. (2009) The Debate on the Pathway of Starch Synthesis: A Closer Look on Low-Starch Mutants Lacking Plastidial Phosphoglucomutase Supports the Chloroplast Localized Pathway. Plant Physiology, 151, 1769-1777.
https://doi.org/10.1104/pp.109.144931

[44]   Hattenbach, A. and Heineke, D. (1999) On the Role of Chloroplastic Phosphoglucomutase in the Regulation of Starch Turn Over. Planta, 207, 527-532.
https://doi.org/10.1007/s004250050513

[45]   Manjunath, S., Lee, C.H.K., VanWinkle, P. and Bailey-Serres, J. (1998) Molecular and Biochemical Characterization of Cytosolic Phosphoglucomutase in Maize Expression during Development and in Response to Oxygen Deprivation. Plant Physiology, 117, 997-1006.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3649683/

[46]   Periappuram, C., Steinhauer, L., Barton, D.L., Taylor, D.C., Chatson, B. and Zou, J. (2000) The Plastidic Phosphoglucomutase from Arabidipsis. A Reversible Enzyme Reaction with an Important Role in Metabolic Control. Plant Physiology, 122, 1193-1199.
https://doi.org/10.1104/pp.122.4.1193

[47]   Harrison, C.J., Mould, R.M., Leech, M.K., Johnson, S.A., Turner, L., Schreck, S.L., Baird, K.M., Jack, P.L., Rawsthorne, S., Hedley, C.L. and Wang, T.L. (2000) The rug3 of Pea Encodes Plastidial Phosphoglucomutase. Plant Physiology, 122, 1187-1192.
https://doi.org/10.1104/pp.122.4.1187

[48]   Rose, D.T., Scherf, U., Eisen, M.B., Perou, C.M., Reese, C., Spellman, P., et al. (2000) Systematic Variation in Gene Expression Patterns in Human Cancer Cell Lines. Nature Genetics, 24, 227-235.
https://doi.org/10.1038/73432

[49]   Grierson. D., Slater, J. and Tucker, G.A. (1985) The Appearance of Polygalacturonase mRNA in Tomatoes. Planta, 163, 263-271.
https://doi.org/10.1007/BF00393517

[50]   Cammaerts, D. and Jacobs, D. (1983) A Study of the Polymorphism and the Genetic Control of the Glutamate Dehydrogenase Isoenzymes in Arabidopsis Thaliana. Plant Science Letters, 31, 67-73.

[51]   Schoppner, A. and Kindl, H. (1984) Purification and Properties of a Stilbene Synthase from Induced Cell Suspension Cultures of Peanut. The Journal of Biological Chemistry, 259, 6806-6811.

[52]   Law, R.D. and Plaxton, W.C. (1995) Purification and Characterization of a Novel Phosphoenolpyruvate Carboxylase from Banana Fruit. Biochemical Journal, 307, 807-816.
https://doi.org/10.1042/bj3070807

[53]   Singal, H.R. and Singh, R. (1986) Purification and Properties of Phosphoenolpyruvate Carboxylase from Immature Pods of Chickpea (Cecer arietium L). Plant Physiology, 80, 369-373.
https://doi.org/10.1104/pp.80.2.369

[54]   Rothermel, B.A. and Nelson, T. (1989) Primary Structure of Maize NADP-Dependent Malic Enzyme. The Journal of Biological Chemistry, 246, 19587-19592.

[55]   Schearer, H.L., Turpin, D.H. and Dennis, D.T. (2004) Characterization of NADP-Dependent Malic Enzyme from Developing Castor Oil Seed Endosperm. Archives of Biochemistry and Biophysics, 429, 134-144.

[56]   Beeching, J.R. and Northcote, D.H. (1987) Nucleic Acid (cDNA) and Amino Acid Sequences of Isocitrate Lyase from Castor Bean. Plant Molecular Biology, 8, 471-475.
https://doi.org/10.1007/BF00017992

[57]   Comai, L., Diewtrich, R.A., Maslyar, D.J., Baden, C.S. and Harada, J.J. (1989) Coordinate Expression of Transcriptionally Regulated Isocitrate Lyase and Malate Synthase Genes in Brassica napus L. The Plant Cell, 1, 293-300.

[58]   Mano, S., Hayashi, M., Kond, S. and Nishimura, M. (1996) cDNA Cloning and Expression of a Gene for Isocitrate Lyase in Pumpkin Cotyledons. Plant and Cell Physiology, 37, 941-948.
https://doi.org/10.1093/oxfordjournals.pcp.a029043

[59]   Grana, X., Broceno, C., Garriga, J., de la Ossa, P.P. and Climent, F. (1993) Phosphoglycerate Mutase Activity and mRNA Levels during Germination of Maize Embryos. Plant Science, 89, 147-151.

[60]   Huang, Y., Blakeley, S.D., McAleese, S.M., Fothergill-Gilmore, L.A. and Dennis, D.T. (1993) Higher Plant Cofactor-Independent Phosphoglyceromutase: Purification, Molecular Characterization and Expression. Plant Molecular Biology, 23, 1039-1053.
https://doi.org/10.1007/BF00021818

[61]   Osvalde, A. (2011) Optimization of Plant Mineral Nutrition Revisited: The Roles of Plant Requirements, Nutrient Interactions, and Soil Properties in Fertilization Management. Environmental and Experimental Biology, 9, 1-8.

[62]   Osuji, G.O. and Breathwaite, C. (1999) Signaling by Glutamate Dehydrogenase in Response to Pesticide Treatment and Nitrogen Fertilization of Peanut. Journal of Agricultural and Food Chemistry, 47, 3332-3344.
https://doi.org/10.1021/jf9805303

[63]   Osuji, G.O. and Madu, W.C. (2015) Glutamate Dehydrogenase. In: D’Mello, J.P.F., Ed., Amino Acids in Higher Plants, Chapter 1, CABI Publishers, Wallingford.

 
 
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