Nitrogen lowers the sulfur amino acid content of soybean (Glycine max [L.] Merr.) by regulating the accumulation of Bowman-Birk protease inhibitor

Journal of Agricultural and Food Chemistry

Volumn 53, Issue 16, 2005, Pages 6347-6354

  Krishnan, Hari B ^a   Bennett, John O ^a   Kim, Won Seok ^a   Krishnan, Ammulu Hari ^a   Mawhinney, Thomas P ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Bowman Birk protease inhibitor; Glycine; Nitrogen; Protein quality; Sulfur amino acids

Indexed keywords

BOWMAN BIRK INHIBITOR; MESSENGER RNA; NITROGEN; SOYBEAN PROTEIN; SULFUR AMINO ACID;

ARTICLE; CELL VACUOLE; CHEMISTRY; DRUG EFFECT; ELECTRON MICROSCOPY; GENE EXPRESSION; GENETICS; PLANT SEED; SOYBEAN; ULTRASTRUCTURE;

AMINO ACIDS, SULFUR; GENE EXPRESSION; MICROSCOPY, ELECTRON; NITROGEN; RNA, MESSENGER; SEEDS; SOYBEAN PROTEINS; SOYBEANS; TRYPSIN INHIBITOR, BOWMAN-BIRK SOYBEAN; VACUOLES;

GLYCINE MAX;

EID: 23844503570     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf050510i     Document Type: Article

References (48)

1. Parsons, C. M.; Potter, L. M.; Brown, R. D. True metabolizable energy and amino acid digestibility of de-hulled soybean meal. Poult. Sci. 1981, 60, 2687-2696.
2. Baidoo, S. K.; Mcintosh, M. K.; Aherne, F. X. Selection preference of starter pigs fed canola meal and soybean meal supplemented diets. Can. J. Anim. Sci. 1986, 66, 1039-1050.
3. Boling, S. D.; Firman, J. D. Digestible sulfur amino acid requirement of starting turkeys. Poult. Sci. 1997, 76, 873-877.
4. Stein, H. H.; Kim, S. W.; Nielsen, T. T.; Easter, R. A. Standardized ileal protein and amino acid digestibility by growing pigs and sows. J. Anim. Sci. 2001, 79, 2113-2122.
5. Karr-Lilienthal, L. K.; Merchen, N. R.; Grieshop, C. M.; Flahaven, M. A.; Mahan, D. C.; Fastinger, N. D.; Watts, M.; Fahey, G. C. Ileal amino acid digestibilities by pigs fed soybean meals from five major soybean-producing countries. J. Anim. Sci. 2004, 82, 3198-3209.
6. Nielsen, N. C. Soybean seed composition. In Soybean: Genetics, Molecular Biology and Biotechnology; Verma, D. P. S., Shoemaker, R. C., Eds.; CAB: Tucson, 1996; pp 127-163.
7. Krishnan, H. B. Biochemistry and molecular biology of soybean seed storage proteins. J. New Seeds 2000, 2, 1-25.
8. Imsande, J. Selection of soybean mutants with increased concentrations of seed methionine and cysteine. Crop Sci. 2001, 41, 510-515.
9. 2 assimilation in oxygenic photosynthesis: The ferredoxin/thioredoxin system. Perspectives on its discovery, present status, and future development. Arch. Biochem. Biophys. 1991, 288, 1-9.
10. May, M. J.; Vernoux, T.; Leaver, C.; Van Montagu, M.; Inzé, D. Glutathione homeostasis in plants: Implications for environmental sensing and plant development J. Exp. Bot. 1998, 49, 649-667.
11. Leustek, T.; Martin, M. N.; Bick, J. A.; Davies, J. P. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51, 141-165.
12. Saito, K.; Takahashi, H.; Noji, M.; Inoue, K.; Hatzfeld, Y. Molecular regulation of sulfur assimilation and cysteine synthesis. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants; Brunold, C., Davidian, J.-C., De Kok, L., Rennenberg, I., Stulen, H., Eds.; Haupt: Bern, Switzerland, 2000; pp 59-72.
13. Leustek, T.; Saito, K. Sulfate transport and assimilation in plants. Plant Physiol. 1999, 120, 637-643.
14. Champigny, M. L. Integration of photosynthetic carbon and nitrogen metabolism in higher plants. Photosynth. Res. 1995, 46, 117-127.
15. Morcuende, R.; Drapp, A.; Hurry, V.; Stitt, M. Sucrose feeding leads to increased rates of nitrate assimilation, increased rates of α-oxoglutarate synthesis, and increased synthesis of a wide spectrum of amino acids in tobacco leaves. Planta 1998, 206, 394-409.
16. Saito, K.; Kurosawa, M.; Tatsuguchi, K.; Takagi, Y.; Murakkoshi, I. Modulation of cysteine biosynthesis in chloroplasts in transgenic tobacco overexpressing cysteine synthase [O-acetylserine(thiol)lyase]. Plant Physiol. 1994, 106, 887-895.
17. Neuenschwander, U.; Suter, M.; Brunold, C. Regulation of sulfate assimilation by light and O-acetylserine in Lemma minor L. Plant Physiol. 1991, 97, 253-258.
18. Holowach, L. P.; Thompson, J. F.; Madison, J. T. Storage protein composition of soybean cotyledons grown in vitro in media of various sulfate concentrations in the presence and absence of exogenous L-methionine. Plant Physiol. 1984, 74, 584-589.
19. Gayler, K. R.; Sykes, G. E. Effects of nutritional stress on the storage proteins of soybeans. Plant Physiol. 1985, 78, 582-585.
20. Pack, N. C.; Imsande, J.; Shoemaker, R. C.; Shibles, R. Nutritional control of soybean seed storage protein. Crop Sci. 1997, 37, 498-503.
21. Sexton, P. J.; Paek, N. C.; Shibles, R. Soybean sulfur and nitrogen balance under varying levels of available sulfur. Crop Sci. 1998a, 38, 975-982.
22. Sexton, P. J.; Naeve, S. L.; Paek, N. C.; Shibles, R. Sulfur availability, cotyledon nitrogen: Sulfur ratio, and relative abundance of seed storage proteins of soybean. Crop Sci. 1998b, 38, 983-986.
23. Ohtake, N.; Suzuki, M.; Takahashi, Y.; Fujiwara, T.; Chino, M.; Ikarashi, T.; Ohyama, T. Differential expression of β-conglycinin genes in nodulated and nonnodulated isolines of soybean. Physiol. Plant. 1996, 96, 101-110.
24. Krishnan, H. B.; Jiang, G.; Krishnan, A. H.; Wiebold, W. J. Seed storage protein composition of nonnodulating soybean (Glycine max (L.) Merr.) and its influence on protein quality. Plant Sci. 2000, 157, 191-199.
25. Kim, H.; Hirai, M. Y.; Hayashi, H.; Chino, M.; Naito, S.; Fujiwara, T. Role of O-acetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta 1999, 209, 282-289.
26. Wilcox, J. R. Sixty years of improvement in publicly developed Elite soybean lines. Crop Sci. 2001, 41, 1711-1716.
27. Yaklich, R. W.; Vinyard, B.; Camp, M.; Douglass, S. Analysis of seed protein and oil from soybean Northern and Southern Region Uniform Tests. Crop Sci. 2002, 42, 1504-1515.
28. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
29. Krishnan, H. B. A simple and rapid method to isolate low molecular weight proteinase inhibitors from soybean. Korean J. Crop Sci. 2004, 49, 342-348.
30. Chrispeels, M. J.; Herman, E. M. Endoplasmic reticulum-derived compartments function in storage and as mediators of vacuolar remodeling via a new type of organelle, precursor protease vesicles. Plant Physiol. 2000, 123, 1227-1233.
31. Kinney, A. J.; Jung, R.; Herman, E. M. Cosuppression of the α-subunits of β-conglycinin in transgenic soybean seeds induces the formation of endoplasmic reticulum-derived protein bodies. Plant Cell 2001, 13, 1165-1178.
32. Mori, T.; Maruyama, N.; Nishizawa, K.; Higasa, T.; Yagasaki, K.; Ishimoto, M.; Utsumi, S. The composition of newly synthesized proteins in the endoplasmic reticulum determines the transport pathways of soybean seed storage proteins. Plant J. 2004, 40, 238-249.
33. Reuveny, Z.; Dougall, D. K.; Trinity, P. M. Regulatory coupling of nitrate and sulfate assimilation pathways in cultured tobacco cells. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 6670-6672.
34. Prosser, I. M.; Purves, J. V.; Saker, L. R.; Clarkson, D. T. Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulfate. J. Exp. Bot. 2001, 52, 113-121.
35. Sunarpi; Anderson, J. W. Effect of nitrogen nutrition on the export of sulphur from leaves in soybean. Plant Soil 1997a, 188, 177-187.
36. Sunarpi; Anderson, J. W. Allocation of S in generative growth of soybean. Plant Physiol. 1997b, 114, 687-693.
37. Nakasathien, S.; Israel, D. W.; Wilson, R. F.; Kwanyuen, P. Regulation of seed protein concentration in soybean by supra-optimal nitrogen supply. Crop Sci. 2000, 40, 1277-1284.
38. Hesse, H.; Nikiforova, V.; Gaklere, B.; Hoefgen, R. Molecular analysis and control of cyseine biosynthesis: Integration of nitrogen and sulfur metabolism. J. Exp. Bot. 2004, 55, 1283-1292.
39. Hirai, M. Y.; Fujiwara, T.; Awazuhara, M.; Kimura, T.; Noji, M.; Saito, K. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 2003, 33, 651-663.
40. Smith, F. W.; Hawkesford, M. J.; Ealing, P. M.; Clarkson, D. T.; Vanden Berg, P. F.; Belcher, A. R.; Warrilow, A. G. Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J. 1997, 12, 875-884.
41. Koprivova, A.; Suter, M.; Op den Camp, R.; Brunold, C.; Kopriva, S. Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol. 2000, 122, 737-746.
42. Anderson, J. W.; Fitzgerald, M. A. Physiological and metabolic origin of sulphur for the synthesis of seed storage proteins. J. Plant. Physiol. 2001, 158, 447-456.
43. Wilcox, J. R. Increasing seed protein in soybean with eight cycles of recurrent selection. Crop Sci. 1998, 38, 1536-1540.
44. Rackis, J. J.; Wolf, W. J.; Baker, E. C. Protease inhibitors in plant foods: Content and inactivation. Adv. Exp. Med. Biol. 1986, 199, 299-347.
45. Biermann, B. J.; de Banzie, J. S.; Handelsman, J.; Thompson, J. F.; Madison, J. T. Methionine and sulfate increases a Bowman-Birk type protease inhibitor and its messenger RNA in soybeans. J. Agric. Food Chem. 1998, 46, 2858-2862.
46. Townsend, J. A.; Thomas, L. A. Factors which influence the Agrobacterium-mediated transformation of soybean. J. Cell Biochem. Suppl. 1994, 18A, abstract X1-014.
47. Dinkins, R. D.; Reddy, M. S. R.; Meurer, C. A.; Yan, B.; Trick, H.; Thibaud-Nissen, F.; Finer, J. A.; Rarrott, W. A.; Collins, G. B. Increased sulfur amino acids in soybean plants overexpressing the maize 15 kDa zein protein. In Vitro Cell Dev. Biol. Plant 2001, 37, 742-747.
48. Kim, W. S.; Krishnan, H. B. Expression of an 11 kDa methionine-rich delta-zein in transgenic soybean results in the formation of two types of novel protein bodies in transitional cells situated between the vascular tissue and storage parenchyma cells. Plant Biotechnol. J. 2004, 2, 199-210.