Soybean Seed Phenolics, Sugars, and Minerals Are Altered by Charcoal Rot Infection in MG III Soybean Cultivars

DOI: 10.4236/fns.2014.519198   PDF   HTML   XML   4,059 Downloads   4,888 Views   Citations

Abstract

Soybean seed is a major source of phytochemical compounds that impact human health nutrition and livestock meal. Charcoal rot is a disease caused by the fungus Macrophomina phaseolina (Tassi) Goid, and thought to infect the plants through roots by a toxin-mediated mechanism, resulting in yield loss and poor seed quality, especially under drought conditions. Limited information is available on the effect of charcoal rot on seed phytochemical compounds and mineral nutrition in soybean. Therefore, the objective of this research was to investigate the effect of charcoal rot infection on seed phenol, seed coat lignin, isoflavones, and minerals using susceptible (S) (DK 3964) and moderately resistant (MR) (AG 3905) maturity group (MG)III soybean cultivars to charcoal rot. A two-year field experiment was conducted, and infested soil with charcoal rot (infested soil conditions, INF) or control (non-infested soil conditions, NINF) was used. The results showed that the moderately resistant genotype had higher concentrations of seed phenolics, total isoflavones, and seed coat lignin under infested and non-infested conditions and under irrigated or non-irrigated conditions compared with the susceptible genotype. The same general trend was found for seed K, Ca, P, Mn, Zn, B, and Cu concentrations in the moderately resistant genotype compared with the susceptible genotype. Our research demonstrated that these seed phytochemical constituents may explain the differences between susceptible and moderately resistant cultivars and may play an important role in the resistance to charcoal rot.

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Bellaloui, N. , Mengistu, A. , Zobiole, L. , Abbas, H. and Kassem, M. (2014) Soybean Seed Phenolics, Sugars, and Minerals Are Altered by Charcoal Rot Infection in MG III Soybean Cultivars. Food and Nutrition Sciences, 5, 1843-1859. doi: 10.4236/fns.2014.519198.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Messina, M.J., Persky, V., Setchell, K.D. and Barnes, S. (1994) Soy Intake and Cancer Risk: A Review of the in Vitro and in Vivo Data. Nutrition and Cancer, 21, 113-131.
http://dx.doi.org/10.1080/01635589409514310
[2] Potter, S.M., Baum, J.A., Teng, H., Stillman, R.J., Shay, N.F., et al. (1998) Soy Protein and Isoflavones: Their Effects on Blood Lipids and Bone Density in Postmenopausal Women. The American Journal of Clinical Nutrition, 68, 1375S-1379S.
[3] Sakthivelu, G., Akitha Devi, M.K., Giridhar, P., Rajasekaran, T., Ravishankar, G.A., et al. (2008) Isoflavone Composition, Phenol Content, and Antioxidant Activity of Soybean Seeds from India and Bulgaria. Journal of Agricultural and Food Chemistry, 56, 2090-2095.
http://dx.doi.org/10.1021/jf072939a
[4] Wikipedia (2013)
http://en.wikipedia.org/wiki/Phenols
[5] Harborne, J.B. (1989) Methods in Plant Biochemistry. In: Dey, P.M. and Harborne, J.B., Eds., Plant Phenolics, Academic Press, London, 283-323.
[6] Lattanzio, V., Veronica, M., Lattanzio, T. and Cardinali, A. (2006) Role of Phenolics in the Resistance Mechanisms of Plants against Fungal Pathogens and Insects In: Imperato, F., Ed., Phytochemistry: Advances in Research, Research Signpost, Kerala, 23-67.
[7] Knaggs, A.R. (2000) The Biosynthesis of Shikimate Metabolites. Natural Product Reports, 18, 334-355.
http://dx.doi.org/10.1039/b001717p
[8] Aoki, T., Akashi, T. and Ayabe, S. (2000) Flavonoids of Leguminous Plants: Structure, Biological Activity, and Biosynthesis. Journal of Plant Research, 113, 475-488.
http://dx.doi.org/10.1007/PL00013958
[9] Whiting, D.A. (2001) Natural Phenolic Compounds 1900-2000: A Bird’s Eye View of a Century’s Chemistry. Natural Product Reports, 18, 583-606.
[10] Wyllie, T.D. (1976) Macrophomina Phaseolina, Charcoal Rot. In: Hill, L.D., Ed., World Soybean Research: Proceedings of the World Soybean Research Conference, Interstate Printers and Publishers Inc., Danville, 482-484.
[11] Mengistu, A., Ray, J.D., Smith, J.R. and Paris, R.L. (2007) Charcoal Rot Disease Assessment of Soybean Genotypes Using a Colony-Forming Unit Index. Crop Science, 47, 2453-2461.
http://dx.doi.org/10.2135/cropsci2007.04.0186
[12] Hill, J.H., Bailey, T.B., Benner, H.I., Tachibana, H. and Durand, D.P. (1987) Soybean Mosaic Virus: Effects of Primary Disease Incidence on Yield and Seed Quality. Plant Disease, 71, 237-239.
http://dx.doi.org/10.1094/PD-71-0237
[13] Mengistu, A. and Heatherly, L.G. (2006) Planting Date, Irrigation, Maturity Group, Year, and Environment Effects on Phomopsis longicolla, Seed Germination, and Seed Health Rating of Soybean in the Early Soybean Production System of the Midsouthern USA. Crop Protection, 25, 310-317.
http://dx.doi.org/10.1016/j.cropro.2005.05.011
[14] Kulik, M.M. and Sinclair, J.B. (1999) Phomposis Seed Decay. In: Hartman, G.L., Sinclair, J.B. and Rupe, J.C., Eds., Compendium of Soybean Diseases, APS Press, The American Phytopathological Society, St. Paul, 31-32.
[15] Siddiqui, K.A., Gupta, A.K., Paul, A.K. and Banerjee, A.K. (1979) Purification and Properties of Heat-Resistant Exotoxin Produced by Macrophomina phaseolina (Tassi) Goid in Culture. Experientia, 35, 1222-1223.
http://dx.doi.org/10.1007/BF01963302
[16] Dhar, T.K., Siddiqui, K.A.I. and Ali, E. (1982) Structure of Phaseolinone, a Novel Phytotoxin from Macrophomina phaseolina. Tetrahedron Letters, 23, 5459-5462.
[17] Ramezani, M., Shier, W.T., Abbas, H.K., Tonos, J.L., Baird, R.E., et al. (2007) Soybean Charcoal Rot Disease Fungus Macrophomina phaseolina in Mississippi Produces the Phytotoxin (-)-Botryodiplodin but No Detectable Phaseolinone. Journal of Natural Products, 70, 28-129.
http://dx.doi.org/10.1021/np060480t
[18] Bellaloui, N., Mengistu, A., Fisher, D.K. and Abel, C.A. (2012) Soybean Seed Composition as Affected by Drought and Phomopsis in Phomopsis Susceptible and Resistant Genotypes. Journal of Crop Improvement, 26, 428-453.
http://dx.doi.org/10.1080/15427528.2011.651774
[19] Smith, G.S. and Wyllie, T.D. (1999) Charcoal Rot. In: Hartman, G.L., Sinclair, J.B. and Rupe, J.C., Eds., Compendium of Soybean Disease, APS Press, American Phytopathological Society, St. Paul, 29-31.
[20] Kendig, S.R., Rupe, J.C. and Scott, H.D. (2000) Effect of Irrigation and Soil Water Stress on Densities of Macrophomina phaseaolina in Soil and Roots of Two Soybean Cultivars. Plant Disease, 84, 895-900.
http://dx.doi.org/10.1094/PDIS.2000.84.8.895
[21] Paris, R.L., Mengistu, A., Tyler, J.M. and Smith, J.R. (2006) Registration of Soybean Germplasm Line DT97-4290 with Moderate Resistance to Charcoal Rot. Crop Science, 46, 2324-2325.
http://dx.doi.org/10.2135/cropsci2005.09.0297
[22] Bellaloui, N., Mengistu, A. and Paris, R.L. (2008) Soybean Seed Composition in Cultivars Differing in Resistance to Charcoal Rot (Macrophomina phaseolina). Journal of Agricultural Sciences, 146, 667-675.
http://dx.doi.org/10.1017/S0021859608007971
[23] Mengistu, A., Smith, J.R., Ray, J.D. and Bellaloui, N. (2011) Seasonal Progress of Charcoal Rot and Its Impact on Soybean Productivity. Plant Disease, 95, 1159-1166.
http://dx.doi.org/10.1094/PDIS-02-11-0100
[24] Kim, S.H., Jung, W.S., Ahn, J.K. and Chung, I.M. (2005) Analysis of Isoflavone Concentration and Composition in Soybean [Glycine max (L.)] Seeds between the Cropping Year and Storage for 3 Years. European Food Research and Technology, 220, 207-214.
http://dx.doi.org/10.1007/s00217-004-1048-5
[25] Riedl, K.M., Lee, J.H., Renita, M., St Martin, S.K., Schwartz, S.J., et al. (2007) Isoflavone Profiles, Phenol Content, and Antioxidant Activity of Soybean Seeds as Influenced by Cultivar and Growing Location in Ohio. Journal of the Science of Food and Agriculture, 87, 1197-1206.
http://dx.doi.org/10.1002/jsfa.2795
[26] Anderson, J.W., Johnstone, B.M. and Cook-Newell, M.E. (1995) Meta-Analysis of the Effects of Soy Protein Intake on Serum Lipids. The New England Journal of Medicine, 333, 276-282.
http://dx.doi.org/10.1056/NEJM199508033330502
[27] Pratt, D.E. and Birac, P.M. (1979) Sources of Antioxidant Activity of Soybeans and Soy Products. Journal of Food Science, 44, 1720-1727.
http://dx.doi.org/10.1111/j.1365-2621.1979.tb09125.x
[28] Hu, H., Brown, P.H. and Labavitch, J.H. (1996) Species Variability in Boron Requirement Is Correlated with Cell Wall Pectin. Journal of ExperimentalBotany, 47, 227-232.
http://dx.doi.org/10.1093/jxb/47.2.227
[29] Moura, J.C., Bonine, C.A., Viana, J.D.O.F., Dornelas, M.C. and Mazzafera, P. (2010) Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants. Journal of Integrated Plant Biology, 52, 360-376.
http://dx.doi.org/10.1111/j.1744-7909.2010.00892.x
[30] Freudenberg, K. and Neish, A.C. (1968) Constitution and Biosynthesis of Lignin. Springer-Verlag, Berlin, 129.
http://dx.doi.org/10.1007/978-3-642-85981-6
[31] Chabannes, M., Ruel, K., Yoshinaga, A., Chabbert, B., Jauneau, A., et al. (2001) In Situ Analysis of Lignins in Transgenic Tobacco Reveals a Differential Impact of Individual Transformations on the Spatial Patterns of Lignin Deposition at the Cellular and Subcellular Levels. Plant Journal, 28, 271-282.
http://dx.doi.org/10.1046/j.1365-313X.2001.01159.x
[32] Wikipedia. Natural Phenol. Accessed on August 9, 2013.
http://en.wikipedia.org/wiki/Natural_phenol
[33] Campbell, M.M. and Sederoff, R.R. (1996) Variation in Lignin Content and Composition (Mechanisms of Control and Implications for the Genetic Improvement of Plants. Plant Physiology, 110, 3-13.
[34] Lewis, N.G. and Yamamoto, E. (1990) Lignin: Occurrence, Biogenesis and Biodegradation. Annual Review of Plant Physiology and Plant Molecular Biology, 41, 455-496.
http://dx.doi.org/10.1146/annurev.pp.41.060190.002323
[35] Krzyzanowski, F.C., Franca-Neto, J.B., Mandarino, J.M.G. and Kaster, M. (2008) Evaluation of Lignin Content of Soybean Seed Coat Stored in a Controlled Environment. Revista Brasileira de Sementes, 30, 220-223.
http://dx.doi.org/10.1590/S0101-31222008000200028
[36] Capeleti, I., Bonini, E.A., Lourdes, M.D., Ferrarese, L., Teixeira, A.C.N., et al. (2005) Lignin Content and Peroxidase Activity in Soybean Seed Coat Susceptible and Resistant to Mechanical Damage. Acta Physiologiae Plantarum, 27, 103-108.
[37] Marschner, H. (1995) Mineral Nutrition of Higher Plants. Academic Press, San Diego, 379-396.
[38] Spann, T.M. and Schumann, A.W. (2010) Mineral Nutrition Contributes to Plant Disease and Pest Resistance. One of a Series of the Horticultural Sciences Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, IFAS Extension, This document is HS1181.
http://edis.ifas.ufl.edu
[39] Graham, N. and Graham, M.Y. (1991) Gyceollinelicitors Induce Major but Distinctly Different Shifts in Isoflavonoid Metabolism in Proximal and Distal Soybean Cell Populations. Molecular Plant-Microbe Interactions, 4, 60-68.
http://dx.doi.org/10.1094/MPMI-4-060
[40] Bolle-Jones, E.W. and Hilton, R.N. (1956) Zinc-Deficiency of Hevea brasiliensis as a Predisposing Factor to Oidium Infection. Nature, 177, 619-620.
http://dx.doi.org/10.1038/177619b0
[41] Schutte, K.H. (1967) The Influence of Boron and Copper Deficiency upon Infection by Erysiphe graminis D.C., the Powdery Mildew, in Wheat var. Kenya. Plant and Soil, 27, 450-452.
http://dx.doi.org/10.1007/BF01376338
[42] Heatherly, L.G., Elmore, C.D., Wesley, R.A. and Spurlock, S.R. (2001) Row Spacing and Weed Management Systems for Non-Irrigated Early Soybean Production System Plantings in the Midsouthern USA. Crop Science, 41, 784-791.
http://dx.doi.org/10.2135/cropsci2001.413784x
[43] Ray, J.D., Heatherly, L.G. and Fritschi, F.B. (2006) Influence of Large Amounts of Nitrogen on Non-Irrigated and Irrigated Soybean. Crop Science, 46, 52-60.
http://dx.doi.org/10.2135/cropsci2005.0043
[44] Alvarez, P.J.C., Krzyzanowski, F.C., Mandarino, J.M.G. and Franca-Neto, J.B. (1997) Relationship between Soybean Seed Coat Lignin Content and Resistance to Mechanical Damage. Seed Science and Technology, 25, 209-214.
[45] Krzyzanowski, F.C., Franca-Neto, J.B., Mandarino, J.M.G. and Kaster, M. (2001) Comparison Between Two Gravimetric Methods to Determine the Lignin Content in Soybean Seed Coat. Seed Science and Technology, 29, 619-624.
[46] Zobiole, L.H.S., Bonini, E.A., Oliveira Jr., R.S., Kremer, R.J. and Ferrarese-Filho, O. (2010) Glyphosate Affects Lignin Content and Amino Acid Production in Glyphosate-Resistant Soybean. Acta Physiologiae Plantarum, 32, 831-837.
[47] Ferrarese, M.L.L., Zottis, A. and Ferrarese-Filho, O. (2002) Protein-Free Lignin Quantification in Soybean (Glycine max) Roots. Biologia, 57, 541-543.
[48] Qin, G.Z. and Tian, S.P. (2005) Enhancement of Biocontrol Activity of Cryptococcus laurentii by Silicon and the Possible Mechanisms Involved. Phytopathology, 95, 69-75.
http://dx.doi.org/10.1094/PHYTO-95-0069
[49] Singleton, V.L. and Rossi, J.A. (1965) Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. American Journal of Enology and Viticulture, 16, 144-158.
[50] Xu, B.J. and Chang, S.K. (2007) A Comparative Study on Phenolic Profiles and Antioxidant Activities of Legumes as Affected by Extraction Solvents. Journal of Food Science, 72, S159-S166.
http://dx.doi.org/10.1111/j.1750-3841.2006.00260.x
[51] Morrison, M.J., Cober, E.R., Saleem, M.F., McLaughlin, N.B., Fregeau-Reid, J., et al. (2008) Changes in Isoflavone Concentration with 58 Years of Genetic Improvement of Short-Season Soybean Cultivars in Canada. Crop Science, 48, 2201-2208.
http://dx.doi.org/10.2135/cropsci2008.01.0023
[52] Sato, T., Eguchi, K., Hatano, T. and Nishiba, Y. (2008) Use of Near-Infra Red Reflectance Spectroscopy for the Estimation of Isoflavone Contents of Soybean Seeds. Plant Production Science, 11, 481-486.
http://dx.doi.org/10.1626/pps.11.481
[53] Wilcox, J.R. and Shibles, R.M. (2001) Interrelationships Among Seed Quality Attributes in Soybean. Crop Science, 41, 11-14.
http://dx.doi.org/10.2135/cropsci2001.41111x
[54] Bellaloui, N., Smith, J.R., Gillen, A.M. and Ray, J.D. (2010) Effect of Maturity on Seed Sugars as Measured on NearIsogenic Soybean (Glycine max) Lines. Crop Science, 50, 1978-1987.
http://dx.doi.org/10.2135/cropsci2009.10.0596
[55] (2012) Sigma USA, Glucose (HK) Assay Kit Product Code GAHK-20. Product Ininformation.
http://www.sigmaaldrich.com/etc/medialib/docs/Sigma/
Bulletin/gahk20bul.Par.0001.File.tmp/gahk20bul.pdf
[56] Bellaloui, N., Hu, Y., Mengistu, A., Kassem, M.A. and Abel, C.A. (2013) Effects of Foliar Boron Application on Seed Composition, Cell Wall Boron, and Seed 15δN and 13δC Isotopes in Water-Stressed Soybean Plants. Frontiers in Plant Science, 4, 1-12.
http://dx.doi.org/10.3389/fpls.2013.00270
[57] (2012) Sigma USA, Fructose Assay Kit, Product Code FA-20. Product Ininformation.
http://www.sigmaaldrich.com/etc/medialib/docs/Sigma/
Bulletin/fa20bul.Par.0001.File.tmp/fa20bul.pdf
[58] Dordas, C. (2006) Foliar Boron Application Improves Seed Set, Seed Yield, and Seed Quality of Alfalfa. Agronomy Journal, 98, 907-913.
http://dx.doi.org/10.2134/agronj2005.0353
[59] Dordas, C., Apostolides, G. and Goundra, O. (2007) Boron Application Affects Seed Yield and Seed Quality of Sugar Beets. Journal of Agricultural Sciences, 145, 377-384.
http://dx.doi.org/10.1017/S0021859607006879
[60] John, M.K., Chuah, H.H. and Neufeld, J.H. (1975) Application of Improved Azomethine-H Method to the Determination of Boron in Soils and Plants. Analytical Letters, 8, 559-568.
http://dx.doi.org/10.1080/00032717508058240
[61] Bandemer, S.L. and Schaible, P.J. (1944) Determination of Iron. A Study of the O-Phenanthroline Method. Industrial and Engineering Chemistry, Analytical Edition, 16, 317-319.
http://dx.doi.org/10.1021/i560129a013
[62] (1959) Analytical Methods Committee, Analysts. Her Majesty’s Stationery Office, London, 84.
[63] Bellaloui, N., Smith, J.R., Gillen, A.M. and Ray, J.D. (2011) Effects of Maturity, Genotypic Background, and Temperature on Seed Mineral Composition in Near-Isogenic Soybean Lines in the Early Soybean Production System. Crop Science, 51, 1161-1171.
http://dx.doi.org/10.2135/cropsci2010.04.0187
[64] Cavell, A.J. (1955) The Colorimetric Determination of Phosphorus in Plant Materials. Journal of the Sciences of Food and Agriculture, 6, 479-480.
http://dx.doi.org/10.1002/jsfa.2740060814
[65] SAS (2001) SAS 9.1 TS LeVel 1M3, Windows Version 5.1.2600. SAS Institute, Cary.
[66] Mengistu, A., Smith, J.R., Bellaloui, N., Paris, R.L. and Wrather, J.A. (2010) Irrigation and Time of Harvest: Effects on Evaluation of Selected Soybean Accessions against Phomopsis longicolla. Crop Science, 50, 2055-2064.
http://dx.doi.org/10.2135/cropsci2009.11.0657
[67] Bellaloui, N., Mengistu, A., Zobiole, L.H.S. and Shier, W.T. (2012) Resistance to Toxin-Mediated Fungal Infection: Role of Lignins, Isoflavones, Other Seed Phenolics, Sugars, and Boron in the Mechanism of Resistance to Charcoal Rot Disease in Soybean. Toxin Reviews, 31, 16-26.
http://dx.doi.org/10.3109/15569543.2012.691150
[68] Dixon, R.A. and Steele, C.L. (1999) Flavonoids and Isoflavonoids—A Gold Mine for Metabolic Engineering. Trends in Plant Science, 4, 394-400.
http://dx.doi.org/10.1016/S1360-1385(99)01471-5
[69] Paxton, J.D. (1980) A New Working Definition of the Term “Phytoalexin”. Plant Disease, 64, 734.
[70] Hu, H. and Brown, P.H. (1994) Localization of Boron in Cell Walls of Squash and Tobacco and its Association with Pectin (Evidence for a Structural Role of Boron in the Cell Wall). Plant Physiolgy, 105, 681-689.
[71] Bellaloui, N. and Brown, P.H. (1998) Cultivar Differences in Boron Uptake and Distribution in Celery (Apium graveolens), Tomato (Lycopersicon esculentum) and Wheat (Triticum aestivum). Plant and Soil, 198, 153-158.
http://dx.doi.org/10.1023/A:1004343031242
[72] Cakmak, I. and Romheld, V. (1997) Boron Deficiency-Induced Impairments of Cellular Functions in Plants. Plant and Soil, 193, 71-83.
http://dx.doi.org/10.1023/A:1004259808322
[73] Bellaloui, N., Reddy, K.N., Gillen, A.M. and Abel, C.A. (2010) Nitrogen Metabolism and Seed Composition as Influenced by Foliar Boron Application in Soybean. Plant and Soil, 336, 143-155.
http://dx.doi.org/10.1007/s11104-010-0455-6
[74] Parr, A.J. and Loughman, B.C. (1983) Boron and Membrane Function in Plants. In: Robb, D.A. and Pierpoint, W.S., Eds., Metals and Micronutrients, Uptake and Utilization by Plants, Academic Press, New York, 87-107.
[75] Lukaszewski, K.M. and Blevins, D.G. (1996) Root Growth Inhibition in Boron-Deficient or Aluminum-Stressed Squash May Be a Result of Impaired Ascorbate Metabolism. Plant Physiolgy, 112, 1135-1140.
[76] Hu, H., Brown, P.H. and Labavitch, J.M. (1996) Species Variability in Boron Requirement Is Correlated with Cell Wall Pectin. Journal of Experimental Botany, 47, 227-232.
http://dx.doi.org/10.1093/jxb/47.2.227
[77] Matoh, T. (1997) Boron in Plant Cell Walls. Plant and Soil, 193, 59-70.
http://dx.doi.org/10.1023/A:1004207824251
[78] Brown, P.H., Bellaloui, N., Wimmer, M.A., Bassil, E.S., Ruiz, J., et al. (2002) Boron in Plant Biology. Plant Biology, 4, 205-223.
http://dx.doi.org/10.1055/s-2002-25740
[79] Cakmak, I., Kurz, H. and Marschner, H. (1995) Short-Term Effects of Boron, Germanium, and High Light Intensity on Membrane Permeability in Boron Deficient Leaves of Sunflower. Physiologia Plantarum, 95, 11-18.
[80] Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., et al. (2002) Important Roles of Drought- and Cold-Inducible Genes for Galactinol Synthase in Stress Tolerance in Arabidopsis thaliana. Plant Journal, 29, 417-426.
http://dx.doi.org/10.1046/j.0960-7412.2001.01227.x
[81] Ren, C., Bilyeu, K.D. and Beuselinck, P.R. (2009) Composition, Vigor, and Proteome of Mature Soybean Seeds Developed under High Temperature. Crop Science, 49, 1010-1022.
http://dx.doi.org/10.2135/cropsci2008.05.0247
[82] Liu, K. (1997) Soybeans Chemistry, Technology, and Utilization. Chapman & Hall, New York.

  
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