Soybean Seed Phenolics, Sugars, and Minerals Are Altered by Charcoal Rot Infection in MG III Soybean Cultivars
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Author(s)
1Crop Genetics Research Unit, USDA-ARS, Stoneville, USA.
2Crop Genetics Research Unit, USDA-ARS, Jackson, USA.
3Crop Protection R & D, Dow AgroSciences—Brazil, Cascavel, Brazil.
4Biological Control of Pests Research Unit, USDA-ARS, Stoneville, USA.
5Plant Genomics and Biotechnology Lab, Department of Biological Sciences, Fayetteville State University, Fayetteville, USA.
2Crop Genetics Research Unit, USDA-ARS, Jackson, USA.
3Crop Protection R & D, Dow AgroSciences—Brazil, Cascavel, Brazil.
4Biological Control of Pests Research Unit, USDA-ARS, Stoneville, USA.
5Plant Genomics and Biotechnology Lab, Department of Biological Sciences, Fayetteville State University, Fayetteville, USA.
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.
KEYWORDS
Cite this paper
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.
| [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. eww141016lx |
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