Effects of proteome rebalancing and sulfur nutrition on the accumulation of methionine rich δ-zein in transgenic soybeans

Frontiers in Plant Science

Volumn 5, Issue November, 2014, Pages 1-12

  Kim, Won Seok ^a   Jez, Joseph M ^b   Krishnan, Hari B ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

7S globulin; Glycine max (L.) Merr; Proteome rebalancing; RNA interference; Sulfur assimilation; zein

Indexed keywords

EID: 84910110701     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00633     Document Type: Article

References (78)

1. Amir, R., Han, T., and Ma, F. (2012). Bioengineering approaches to improve the nutritional values of seeds by increasing their methionine content. Mol. Breed. 29, 915-924. doi: 10.1007/s11032-011-9690-7.
2. Amira, G., Ifat, M., Tal, A., Hana, B., Shmuel, G., and Rachel, A. (2005). Soluble methionine enhances accumulation of a 15 kDa zein, a methionine-rich storage protein, in transgenic alfalfa but not in transgenic tobacco plants. J. Exp. Bot. 56, 2443-2452. doi: 10.1093/jxb/eri237.
3. Avraham, T., Badani, H., Galili, S., and Amir, R. (2005). Enhanced levels of methionine and cysteine in transgenic alfalfa (Medicago sativa L.) plants over-expressing the Arabidopsis cystathionine ϒ-synthase gene. Plant Biotech. J. 3, 71-79. doi: 10.1111/j.1467-7652.2004.00102.x.
4. Beilinson, V., Chen, Z., Shoemaker, C., Fischer, L., Goldberg, B., and Nielsen, C. (2002). Genomic organization of glycinin genes in soybean. Theor. Appl. Genet. 104, 1132-1140. doi: 10.1007/s00122-002-0884-6.
5. Bilyeu, K. D., Zeng, P., Coello, P., Zhang, Z. J., Krishnan, H. B., Bailey, A., et al. (2008). Quantitative conversion of phytate to inorganic phosphorus in soybean seeds expressing a bacterial phytase. Plant Physiol. 146, 468-477. doi: 10.1104/pp.107.113480.
6. Bost, K., and Piller, K. (2011). "Protein expression systems: why soybean seeds? " in Soybean-Molecular Aspects of Breeding ISBN: 978-953-307-240-1, ed A. Sudaric (Rijeka: InTech), 1-18. doi: 10.5772/15376.
7. Chiaiese, P., Ohkama-Ohtsu, N., Molvig, L., Godfree, R., Dove, H., Hocart, C., et al. (2004). Sulphur and nitrogen nutrition influence the response of chickpea seeds to an added, transgenic sink for organic sulphur. J. Exp. Bot. 55, 1889-1901. doi: 10.1093/jxb/erh198.
8. Coates, J. B., Medeiros, J. S., Thanh, V. H., and Nielsen, N. C. (1985). Characterization of the subunits of β-conglycinin. Arch. Biochem. Biophys. 243, 184-194. doi: 10.1016/0003-9861(85)90787-8.
9. Cunha, N. B., Araujo, A. C. G., Leite, A., Murad, A. M., Vianna, G. R., and Rech, E. L. (2010). Correct targeting of proinsulin in protein storage vacuoles of transgenic soybean seeds. Genet. Mol. Res. 9, 1163-1170. doi: 10.4238/vol9-2gmr849.
10. Dancs, G., Kondrák, M., and Bánfalvi, Z. (2008). The effects of enhanced methionine synthesis on amino acid and anthocyanin content of potato tubers. BMC Plant Biol. 8:65 doi: 10.1186/1471-2229-8-65.
11. Ding, S. H., Huang, L. Y., Wang, Y. D., Sun, H. C., and Xiang, Z. H. (2006). High-level expression of basic fibroblast growth factor in transgenic soybean seeds and characterization of its biological activity. Biotechnol. Lett. 28, 869-875. doi: 10.1007/s10529-006-9018-6.
12. Dinkins, R. D., Reddy, R., Meurer, C. A., Yan, B., Trick, H., Thibaud-Nissen, F., et al. (2001). Increased sulfur amino acids in soybean plants overexpressing the maize 15 kD zein protein. In Vitro Cell. Dev. Biol. Plant 37, 742-747. doi: 10.1007/s11627-001-0123-x.
13. Fehr, W. R., Caviness, C. E., Burmood, D. T., and Pennington, J. S. (1971). Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci. 11, 929-931. doi: 10.2135/cropsci1971.0011183X001100060051x.
14. Friedman, A. M., Long, S. R., Brown, S. E., Buikema, W. J., and Ausubel, F. M. (1982). Construction of broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene 18, 289-296. doi: 10.1016/0378-1119(82)90167-6.
15. Frizzi, A., Caldo, R. A., Morrell, J. A., Wang, M., Lutfiyya, L. L., Brown, W. E., et al. (2010). Compositional and transcriptional analyses of reduced zein kernels derived from the opaque2 mutation and RNAi suppression. Plant Mol. Biol. 73, 569-585. doi: 10.1007/s11103-010-9644-1.
16. Galili, G., and Amir, R. (2013). Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality. Plant Biotech. J. 11, 211-222. doi: 10.1111/pbi.12025.
17. Garg, R., Tolbert, M., Oakes, J. L., Clemente, T. E., Bost, K. L., and Piller, K. J. (2007). Chloroplast targeting of FanC, the major antigenic subunit of Escherichia coli K99 fimbriae, in transgenic soybean. Plant Cell Rep. 26, 1011-1023. doi: 10.1007/s00299-007-0322-y.
18. Gayler, K. R., and Sykes, G. E. (1985). Effects of nutritional stress on the storage proteins of soybeans. Plant Physiol. 78, 582-585. doi: 10.1104/pp.78.3.582.
19. Goossens, A., Van Montagu, M., and Angenon, G. (1999). Co-introduction of an antisense gene for an endogenous seed storage protein can increase expression of a transgene in Arabidopsis thaliana seeds. FEBS Lett. 456, 160-164. doi: 10.1016/S0014-5793(99)00943-6.
20. Hacham, Y., Avraham, T., and Amir, R. (2002). The N-terminal region of Arabidopsis cystathionine ϒ-synthase plays an important regulatory role in methionine metabolism. Plant Physiol. 128, 454-462. doi: 10.1104/pp.010819.
21. Hagan, N. D., Upadhyaya, N., Tabe, L. M., and Higgins, T. J. (2003). The redistribution of protein sulfur in transgenic rice expressing a gene for a foreign, sulfur-rich protein. Plant J. 34, 1-11. doi: 10.1046/j.1365-313X.2003.01699.x.
22. Harada, J. J., Baker, S. J., and Goldberg, R. B. (1989). Soybean beta-conglycinin genes are clustered in several DNA regions and are regulated by transcriptional and posttranscriptional processes. Plant Cell 1, 415-425.
23. Hawkesford, M. J. (2000). Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J. Exp. Bot. 51, 131-138. doi: 10.1093/jexbot/51.342.131.
24. Hawkesford, M. J., and De Kok, L. J. (2006). Managing sulphur metabolism in plants. Plant Cell Environ. 29, 382-395. doi: 10.1111/j.1365-3040.2005.01470.x.
25. Hayashi, M., Harada, K., Fujiwara, T., and Kitamura, K. (1998). Characterization of a 7S globulin-deficient mutant of soybean (Glycine max (L.) Merrill). Mol. Genet. Genomics 258, 208-214. doi: 10.1007/s004380050724.
26. Herman, E. M. (2014). Soybean seed proteome rebalancing. Front. Plant Sci. 5:437. doi: 10.3389/fpls.2014.00437.
27. Hinchee, M. A. W., Connor-Ward, D. V., Newell, C. A., McDonnell, R. E., Sato, S. J., Gasser, C. S., et al. (1988). Production of transgenic soybean plants using Agrobacterium -mediated DNA transfer. Biotechnology 6, 915-922. doi: 10.1038/nbt0888-915.
28. Kim, W. S., Chronis, D., Juergens, M., Schroeder, A. C., Hyun, S. W., Jez, J. M., et al. (2012). Transgenic soybean plants overexpressing O -acetylserine sulfhydrylase accumulate enhanced levels of cysteine and Bowman-Birk protease inhibitor in seeds. Planta 235, 13-23. doi: 10.1007/s00425-011-1487-8.
29. Kim, W. S., and Krishnan, H. B. (2003). Allelic variation and differential expression of methionine-rich δ-zeins in maize inbred lines B73 and W23a1. Planta 217, 66-74. doi: 10.1007/s00425-002-0971.
30. Kim, W. S., and Krishnan, H. B. (2004). 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 Biotech. J. 2, 199-210. doi: 10.1111/j.1467-7652.2004.00063.x.
31. Kitamura, K., and Kaizuma, N. (1981). Mutant strains with low level of subunits of 7S globulin in soybean (Glycine max Merr.) seed. Jpn. J. Breed. 31, 353-359. doi: 10.1270/jsbbs1951.31.353.
32. Kopriva, S., Suter, M., von Ballmoos, P., Hesse, H., Krähenbühl, U., Rennenberg, H., et al. (2002). Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol. 130, 1406-1413. doi: 10.1104/pp.007773.
33. Krishnan, H. B. (2000). Biochemistry and molecular biology of soybean seed storage proteins. J. New Seeds 2, 1-25. doi: 10.1300/J153v02n03_01.
34. Krishnan, H. B. (2005). Engineering soybean for enhanced sulfur amino acid content. Crop Sci. 45, 454-461. doi: 10.2135/cropsci2005.0454.
35. Krishnan, H. B., and Nelson, R. L. (2011). Proteomic analysis of high protein soybean (Glycine max ) accessions demonstrates the contribution of novel glycinin subunits. J. Agric. Food Chem. 59, 2432-2439. doi: 10.1021/jf104330n.
36. Krishnan, H. B., Oehrle, N. W., and Natarajan, S. S. (2009). A rapid and simple procedure for the depletion of abundant storage proteins from legume seeds to advance proteome analysis: a case study using Glycine max. Proteomics 9, 3174-3188. doi: 10.1002/pmic.200800875.
37. Lange, M., Vincze, E., Wieser, H., Schjørring, J. K., and Holm, P. B. (2007). Effect of an antisense C-hordein gene on the storage protein composition in the barley seed. J. Agric. Food Chem. 55, 6074-6081. doi: 10.1021/jf0709505.
38. Lee, J. D., Woolard, M., Sleper, D. A., Smith, J. R., Pantalone, V. R., Nyinyi, C. N., et al. (2009). Environmental effects on oleic acid in soybean seed oil of plant introductions with elevated oleic concentration. Crop Sci. 49, 1762-1768. doi: 10.2135/cropsci2008.11.0663.
39. Lin, Y., Pajak, A., Marsolais, F., McCourt, P., and Riggs, C. D. (2013). Characterization of a cruciferin deficient mutant of Arabidopsis and its utility for overexpression of foreign proteins in plants. PLoS ONE 8:e64980. doi: 10.1371/journal.pone.0064980.
40. Marsolais, F., Pajak, A., Yin, F., Taylor, M., Gabriel, M., Merino, D. M., et al. (2010). Proteomic analysis of common bean seed with storage protein deficiency reveals up-regulation of sulfur-rich proteins and starch and raffinose metabolic enzymes, and down-regulation of the secretory pathway. J. Proteomics 73, 1587-1600. doi: 10.1016/j.jprot.2010.03.013.
41. Matamoros, M. A., Moran, J. F., Iturbe-Ormaetxe, I., Rubio, M. C., and Becana, M. (1999). Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol. 121, 879-888. doi: 10.1104/pp.121.3.879.
42. Moravec, T., Schmidt, M. A., Herman, E. M., and Woodford-Thomas, T. (2007). Production of Escherichia coli heat labile toxin (LT) B subunit in soybean seed and analysis of its immunogenicity as an oral vaccine. Vaccine 25, 1647-1657. doi: 10.1016/j.vaccine.2006.11.010.
43. Nielsen, N. C. (1996). "Soybean seed composition," in Soybean: Genetics, Molecular Biology and Biotechnology, eds D. P. S. Verma and R. C. Shoemaker (Wallingford: CABI), 127-163.
44. Nielsen, N. C., Dickinson, C. D., Cho, T. J., Thanh, V. H., Scallon, B. J., Fischer, R. L., et al. (1989). Characterization of the glycinin gene family in soybean. Plant Cell 1, 313-328. doi: 10.1105/tpc.1.3.313.
45. Nielsen, N. C., and Nam, Y. W. (1999). "Soybean globulins," in Seed Proteins, eds P. R. Shewry and R. Casey (Dordrecht: Kluwer Academic Publishers), 285-313. doi: 10.1007/978-94-011-4431-5_13.
46. Odanaka, H., and Kaizuma, N. (1989). Mutants on soybean storage proteins induced with γ-ray irradiation. Jpn. J. Breed. 39, 430-431.
47. Ogawa, T., Tayama, E., Kitamura, K., and Kaizuma, N. (1989). Genetic improvement of seed storage protein using three variant alleles of 7S globulin subunits in soyabean. (Glycine max L.). Jpn. J. Breed. 39, 137-147. doi: 10.1270/jsbbs1951.39.137.
48. Panthee, D. R., Kwanyuen, P., Sams, C. E., West, D. R., Saxton, A. M., and Pantalone, V. R. (2004). Quantitative trait loci for β-conglycinin (7S) and glycinin (11S) fractions of soybean storage protein. J. Am. Oil Chem. Soc. 81, 1005-1012. doi: 10.1007/s11746-004-1014-4.
49. Piller, K. J., Clemente, T. E., Jun, S. M., Petty, C. C., Sato, S., Pascual, D. W., et al. (2005). Expression and immunogenicity of an Escherichia coli K99 fimbriae subunit antigen in soybean. Planta 222, 6-18. doi: 10.1007/s00425-004-1445-9.
50. Rao, S. S., and Hildebrand, D. (2009). Changes in oil content of transgenic soybeans expressing the yeast SLC1 gene. Lipids 44, 945-951. doi: 10.1007/s11745-009-3337-z.
51. Scherer, H. W., Pacyna, S., Spoth, K. R., and Schulz, M. (2008). Low levels of ferredoxin, ATP and leghemoglobin contribute to limited N2 fixation of Peas (Pisum sativum L.) and alfalfa (Medicago sativa L.) under S deficiency conditions. Biol. Fertil. Soils 44, 909-916. doi: 10.1007/s00374-008-0273-7.
52. Schmidt, M. A., Barbazuk, W. B., Sandford, M., May, G., Song, Z., Zhou, W., et al. (2011). Silencing of soybean seed storage proteins results in a rebalanced protein composition preserving seed protein content without major collateral changes in the metabolome and transcriptome. Plant Physiol. 156, 330-345. doi: 10.1104/pp.111.173807.
53. Schmidt, M. A., and Herman, E. M. (2008). Proteome rebalancing in soybean seeds can be exploited to enhance foreign protein accumulation. Plant Biotech. J. 6, 832-842. doi: 10.1111/j.1467-7652.2008.00364.x.
54. Scossa, F., Laudencia-Chingcuanco, D., Anderson, O. D., Vensel, W. H., Lafiandra, D., D'Ovidio, R., et al. (2008). Comparative proteomic and transcriptional profiling of a bread wheat cultivar and its derived transgenic line overexpressing a low molecular weight glutenin subunit gene in the endosperm. Proteomics 8, 2948-2966. doi: 10.1002/pmic.200700861.
55. Segal, G., Song, R. T., and Messing, J. (2003). A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165, 387-397.
56. Shewry, P. R. (2000). "Seed proteins," in Seed Technology and its Biological Basis, eds M. Black and J. D. Bewley (Sheffield: Sheffield Academic Press), 42-84.
57. Shigemitsu, T., Ozaki, S., Saito, Y., Kuroda, M., Morita, S., Satoh, S., et al. (2012). Production of human growth hormone in transgenic rice seeds: co-introduction of RNA interference cassette for suppressing the gene expression of endogenous storage proteins. Plant Cell Rep. 31, 539-549. doi: 10.1007/s00299-011-1191-y.
58. Song, S., Hou, W., Godo, I., Wu, C., Yu, Y., Matityahu, I., et al. (2013). Soybean seeds expressing feedback-insensitive cystathionine-γ-synthase exhibit a higher content of methionine. J. Exp. Bot. 64, 1917-1926. doi: 10.1093/jxb/ert053.
59. Spencer, D., Rerie, W., Randall, P., and Higgins, T. (1990). The regulation of pea seed storage protein genes by sulfur stress. Funct. Plant Biol. 17, 355-363.
60. Staswick, P., Hermodson, M. A., and Nielsen, N. C. (1984). Identification of the cystines which link the acidic and basic components of the glycinin subunits. J. Biol. Chem. 259, 13431-13435.
61. Streatfield, S. J. (2007). Approaches to achieve high-level heterologous protein production in plants. Plant Biotech. J. 5, 2-15. doi: 10.1111/j.1467-7652.2006.00216.x.
62. Tabe, L., Hagan, N., and Higgins, T. J. (2002). Plasticity of seed protein composition in response to nitrogen and sulfur availability. Curr. Opin. Plant Biol. 5, 212-217. doi: 10.1016/S1369-5266(02)00252-2.
63. Tabe, L. M., and Droux, M. (2001). Sulfur assimilation in developing lupin cotyledons could contribute significantly to the accumulation of organic sulfur reserves in the seed. Plant Physiol. 126, 176-187. doi: 10.1104/pp.126.1.176.
64. Tabe, L. M., and Higgins, T. J. (1998). Engineering plant protein composition for improved nutrition. Trends Plant Sci. 3, 282-286. doi: 10.1016/S1360-1385(98)01267-9.
65. Tabe, L. M., Wirtz, M., Molvig, L., Droux, M., and Hell, R. (2010). Overexpression of serine acetlytransferase produced large increases in O -acetylserine and free cysteine in developing seeds of a grain legume. J. Exp. Bot. 61, 721-733. doi: 10.1093/jxb/erp338.
66. Tada, Y., Utsumi, S., and Takaiwa, F. (2003). Foreign gene products can be enhanced by introduction into low storage protein mutants. Plant Biotech. J. 1, 411-422. doi: 10.1046/j.1467-7652.2003.00038.x.
67. Takahashi, K., Banba, H., Kikuchi, A., Ito, M., and Nakamura, S. (1994). An induced mutant line lacking the α-subunit of β-conglycinin in soybean (Glycine max (L.) Merrill). Jpn. J. Breed. 44, 65-66. doi: 10.1270/jsbbs1951.44.65.
68. Takahashi, M., Uematsu, Y., Kashiwaba, K., Yagasaki, K., Hajika, M., Matsunaga, R., et al. (2003). Accumulation of high levels of free amino acids in soybean seeds through integration of mutations conferring seed protein deficiency. Planta 217, 577-586. doi: 10.1007/s00425-003-1026-3.
69. Taylor, M., Chapman, R., Beyaert, R., Hernández-Sebastià, C., and Marsolais, F. (2008). Seed storage protein deficiency improves sulfur amino acid content in common bean (Phaseolus vulgaris L.): redirection of sulfur from gamma-glutamyl-S-methyl-cysteine. J. Agric. Food Chem. 56, 5647-5654. doi: 10.1021/jf800787y.
70. Thanh, V. H., and Shibasaki, K. (1978). Major proteins of soybean seeds. subunit structure of β-conglycinin. J. Agric. Food Chem. 26, 692-695. doi: 10.1021/jf60217a026.
71. Townsend, J. A., and Thomas, L. A. (1994). Factors which influence the Agrobacterium -mediated transformation of soybean. J. Cell Biochem. Supp. 18A, 78-86.
72. Varin, S., Cliquet, J. B., Personeni, E., Avice, J. C., and Lemauviel-Lavenant, S. (2010). How does sulphur availability modify N acquisition of white clover (Trifolium repens L.)? A J. Exp. Bot. 61, 225-234. doi: 10.1093/jxb/erp303.
73. Wesley, S. V., Helliwell, C. A., Smith, N. A., Wang, M., Rouse, D. T., Liu, Q., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581-590. doi: 10.1046/j.1365-313X.2001.01105.x.
74. Yagasaki, K., Kaizuma, N., and Kitamura, K. (1996). Inheritance of glycinin subunits and characterization of glycinin molecules lacking the subunits in soybean (Glycine max (L.) Merr.). Breeding Sci. 46, 11-15.
75. Zhang, Z., Xing, A., Staswick, P. E., and Clemente, T. (1999). The use of glufosinate as a selective agent inAgrobacterium -mediated transformation of soybean. Plant Cell Tiss. Org. 37, 37-46. doi: 10.1023/A:1006298622969.
76. Zhao, F. J., Hawkesford, M. J., and McGrath, S. P. (1999a). Sulphur assimilation and effects on yield and quality of wheat. J. Cereal Sci. 30, 1-17. doi: 10.1006/jcrs.1998.0241.
77. Zhao, F. J., Wood, A. P., and McGrath, S. P. (1999b). Effects of sulphur nutrition on growth and nitrogen fixation of pea (Pisum sativum L.). Plant Soil 212, 207-217. doi: 10.1023/A:1004618303445.
78. Zuber, H., Poignavent, G., Le Signor, C., Aimé, D., Vieren, E., Tadla, C., et al. (2013). Legume adaptation to sulfur deficiency revealed by comparing nutrient allocation and seed traits in Medicago truncatula. Plant J. 76, 982-996. doi: 10.1111/tpj.12350.