Research Advances and Application of Agrobacterium-mediated Transformation in Soybean

doi:10.11924/j.issn.1000-6850.casb15080113

Abstract

Abstract: Genetic transformation of soybean (Glycine max (L.) Merr) depends mainly on Agrobacterium mediation system. In recent years, the soybean genetic transformation has been developed rapidly, but there are still some problems such as lack of genotypes, low transformation efficiency, imperfect regeneration system and so on. In order to explore the main problems and strategies of soybean genetic transformation, in this review, the author introduced the modifications of the technical procedures including the selection of genotypes and explants, strains screening, marker gene selection and medium composition, in order to obtain effective solutions. And the author also introduced the application of the Agrobacterium-mediated soybean transformation in crop improvement and functional genomics.

Yao Bingchen,Sun Yue,Sun Linjing,Su Jingping,Yan Shuangyong and Liu Xuejun. Research Advances and Application of Agrobacterium-mediated Transformation in Soybean[J]. Chinese Agricultural Science Bulletin, 2016, 32(6): 24-33.

References

[1] 蔡一荣.农杆菌介导的高油酸大豆遗传转化方法的建立[D].长春:东北师范大学, 2006.
[2] Pedersen H C, Christiansen J, Wyndaele R. Induction and in vitro culture of soybean crown gall tumors[J]. Plant Cell Report, 1983,2(4): 201-204.
[3] Hinchee M A W, Conner-Ward D V, Newell C A, et al. Fraley and R.B.Horsch. Production of transgenic soybean plants using Agrobacterium-mediated DNA transfer [J]. Nature Biotechnology, 1988 6: 915-922.
[4] Parrott W A, Dryde G, Vogt S, et al. Optimization of somatic embryogenesis and embryo germination in soybean [J]. In Vitro Cellular & Developmental Biology-Plant, 1988, 24(8): 817-820.
[5] Owens L D, Cress D E. Genotypic variability of soybean response to Agrobacterium strains harboring Ti or Ri plasmids [J]. Plant Physiology, 1985, 77(1): 87-94.
[6] McKenzie M A, Cress D E. The evaluation of South African cultivars of soybean for their susceptibility to Agrobacterium tumefaciens and the production of transgenic soybean [J]. South African Journal of Science, 1992, 88(4): 1993-196.
[7] Bailey M A, Boerma H R, Parrott W A. Inheritance of tumor formation in response to Agrobacterium tumefaciens in soybean [J].Crop Science, 1994: 34(2):514-519.
[8] Bodanese D A, Zanetti M H, Mundstock E, et al. Susceptibility of Brazilian soybean cultivars to Agrobacterium tumefaciens [J]. Brazilian Journal of Genetics, 1994, 17(1): 83-88.
[9] Cheng T Y, Saka T, Voqui-Dinh T H. Plant regeneration from soybean cotyledonary node segments in culture [J]. Plant Science Letters, 1980,19(2):91-99.
[10] Trick H N, Finer J J. Sonication-assisted Agrobacterium mediated transformation of soybean [Glycine max (L.) Merrill] embryogenic suspension culture tissue [J]. Plant Cell Report, 1998, 17(6): 482-488.
[11] Olhoft P M, Flagel L E, Donovan C M, et al. Efficient soybean transformation using hygromycin B selection in the cotyledonary-node method [J]. Planta, 2003, 216(5): 723-735.
[12] Olhoft P M, Lin K, Galbraith J, et al. The role of thiol compounds in increasing Agrobacterium-mediated transformation of soybean cotyledonary-node cells [J]. Plant Cell Report, 2001, 20(8): 731-737.
[13] Paz M M, Shou H, Guo Z, et al. Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explants [J]. Euphytica, 2004, 136(2): 167-179.
[14] Santarém E R, Trick H N, Essig J S, et al. Sonication-assisted Agrobacterium-mediated transformation of soybean immature cotyledons: optimization of transient expression [J].Plant Cell Report,1998, 17(10): 752-759.
[15] Bodanese D A, Zanetti M H, Mundstock E, et al. Susceptibility of Brazilian soybean cultivars to Agrobacterium tumefaciens [J]. Brazilian Journal of Genetics, 1994, 17(1):83-88.
[16] Danaldson P A, Simmonds D H. Susceptibility to Agrobacterium tumefaciens and cotyledonary node transformation in short-season soybean [J].Plant Cell Report, 2000, 19(5):478-484.
[17] Meurer C A, Dinkins R D, Collins G B. Factors affecting soybean cotyledonary node transformation[J]. Plant Cell Report,1998, 18(3-4):180-186.
[18] Zhang Z, Xing A, Staswick P, et al. The use of glufosinate as a selective agent in Agrobacterium-mediated transformation of soybean[J]. Plant Cell Tissue Organ Culture, 1999 56(1):37-46.
[19] Olhoft P M, Somers D A. L-Cysteine increases Agrobacterium-mediated T-DNA delivery into soybean cotyledonary-node cells [J]. Plant Cell Report, 2001, 20(8): 706-711.
[20] Liu H K, Yang C, Wei Z M. Efficient Agrobacterium tumefaciens-mediated transformation of soybeans using an embryonic tip regeneration system [J]. Planta, 2004, 219(6): 1042-1049.
[21] Olhoft P M, Flagel L E, Somers D A. T-DNA locus structure in a large population of soybean plants transformed using the Agrobacterium-mediated cotyledonary-node method [J]. Plant Biotechnology Journal, 2004, 2(4): 289-300.
[22] Paz M M, Martinez J C, Kalvig A B, et al. Improved cotyledonary node method using an alternative explant derived from mature seed for efficient Agrobacterium-mediated soybean transformation [J]. Plant Cell Report, 2006, 25(3): 206-213.
[23] Yamada T, Watanabe S, Arai M. Cotyledonary node pre-wounding with a micro-brush increased frequency of Agrobacterium-mediated transformation in soybean[J]. Plant Biotechnology, 2010, 27(2):217-220.
[24] 党尉,卫志明.根癌农杆菌介导的高效大豆遗传转化体系的建立[J].分子细胞生物学报, 2007,3:185-195.
[25] 李小平,马媛媛,李鹏丽,等.利用RNA干扰技术敲rlpk2基因的表达可以延缓大豆叶片衰老[J].科学通报,2005,11(50):1090-1097.
[26] 马丽萍,胡正,张保缺,等.一种快速、高效的大豆农杆菌转化技术[J].中国农业科学, 2008,41(3):661-668.
[27] Hong H P, Zhang H Y, Olhoft P M, et al. Organogenic callus as the target for plant regeneration and transformation via Agrobacterium in soybean (Glycine max (L.) Merr.)[J]. In Vitro Cellular & Developmental Biology-Plant, 2007, 43(6): 558-568.
[28] Gao X R, Wang G K, Su Q, et al. Phytase expression in transgenic soybeans: Stable transformation with a vector-less construct [J]. Biotehnology Letters, 2007, 29:1757-178.
[29] Wang G L, Xu Y N. Hypocotyl-based Agrobacterium-mediated transformation of soybean (Glycine max) and application for RNA interference[J]. Plant Cell Reports, 2008, 27(7): 1177-1184.
[30] 马晓红,姚陆铭,武天龙.大豆整个子叶节外植体再生体系的建立及与子叶节、胚尖再生体系的比较[J].大豆科学,2008,27(3):373-390.
[31] Liu J F, Su Q, An L J, et al. Transfer of a minimal linear marker-free and vector-flee smGFP cassette into soybean via ovary-drip transformation[J]. Biotehnology Letters, 2009, 31(2): 295-30.
[32] 王翠艳,丁东风,于晓菊,等. Floral dip法在大豆遗传转化中的应用研究[J].南开大学学报:自然科学版, 2010,1:36-40.
[33] 王罡,王萍,蔺宇,等.大豆基因型对根癌农杆菌菌株敏感性的研究[J].遗传, 2002,24(5):297-300.
[34] Bush A L, Pueppke S G. Characterization of an unusual new Agrobacterium tumefaciens strain from Chrysanthemum moriflorium Ram[J]. Appl. Environm. Microbiol., 1991,57: 2468-2472.
[35] Torisky R, Kovacs L, Avdiushko S, et al. Development of a binary vector system for plant transformation based on the supervirulent Agrobacterium tumefaciens strain Chry5 [J]. Plant Cell Report, 1997, 17(2): 102-108.
[36] Ko T S, Lee S, Farrand S K, et al. A partially disarmed vir helper plasmid, pKYRT1, in conjunction with 2,4-dichlorophenoxyactic acid promotes emergence of regenerable transgenic somatic embryos from immature cotyledons of soybean [J]. Planta, 2004, 218(4): 536-541.
[37] Dang W, Wei Z. An optimized Agrobacterium-mediated transformation for soybean for expression of binary insect resistance genes [J]. Plant Science, 2007, 173(4): 381-389.
[38] Donaldson P A, Simmonds D H. Susceptibility to Agrobacterium tumefaciens and cotyledonary node transformation in short-season soybean [J]. Plant Cell Report, 2000, 19(5): 478-484.
[39] Zeng P, Vadnais D A, Zhang Z, et al. Refined glufosinate selection in Agrobacterium-mediated transformation of soybean [Glycine max (L.) Merrill] [J]. Plant Cell Report, 2004, 22(7): 478-482
[40] Xue R G, Xie H F, Zhang B. A multi-needle-assisted transformation of soybean cotyledonary node cells [J]. Biotechnology Letters, 2006, 28(19): 1551-1557.
[41] Sato H, Yamada T, Kita Y, et al. Production of transgenic plants and their early seed set in Japanese soybean variety, Kariyutaka [J]. Plant Biotechnology, 2007, 24(5): 533-536.
[42] Yamada T, Watanabe S, Arai M, et al. Cotyledonary node pre-wounding with a micro-brush increased frequency of Agrobacterium-mediated transformation in soybean [J]. Plant Biotechnology, 2010, 27(2): 217-220.
[43] Liu S J, Wei Z M, Huang J Q. The effect of cocultivation and selection parameters on Agrobacterium-mediated transformation of Chinese soybean varieties [J]. Plant Cell Report,2008, 27(3): 489-498.
[44] Parrott W A, Hoffman L M, Hildebrand D F, et al. Recovery of primary transformants of soybean [J]. Plant Cell Report,1989, 7(8): 615-617.
[45] McCabe D E, Swain W F, Martinell B J, et al. Stable transformation of soybean (Glycine max) by particle acceleration [J]. Nature Biotechnology, 1988, 6: 923-926.
[46] Arag?o F J L, Sarokin L, Vianna G R, et al. Selection of transgenic meristematic cells utilizing a herbicidal molecule results in the recovery of fertile transgenic soybean [Glycine max (L.) Merril] plants at a high frequency [J]. Theoretical and Applied Genetics, 2000, 101(1): 1-6.
[47] Finer J J, McMullen M D. Transformation of soybean via particle bombardment of embryogenic suspension culture tissue [J]. In Vitro Cellular & Developmental Biology-Plant, 1991, 27($): 175-182.
[48] Sato S, Newell C, Kolacz K, et al. Stable transformation via particle bombardment in two different soybean regeneration systems [J]. Plant Cell Report, 1993, 12(7): 408-413.
[49] Parrott W A, All J N, Adang M J, et al. Recovery and evaluation of soybean plants transgenic for a Bacillus thuringiensis var. Kurstaki insecticidal gene [J]. In Vitro Cellular & Developmental Biology-Plant, 1994, 30(3): 144-149.
[50] Stewart C N J, Adang M J, All J N, et al. Genetic transformation, recovery, and characterization of fertile soybean transgenic for a synthetic Bacillus thuringiensis cryIAc gene [J]. Plant Physiology, 1996, 112(1): 121-129.
[51] Maughan P J, Philip R, Cho M J, et al. Biolistic transformation, expression, and inheritance of bovine β-casein in soybean (Glycine max) [J]. In Vitro Cellular & Developmental Biology-Plant, 1999, 35(4): 344-349.
[52] Reddy M S S, Dinkins R D, Collins G B. Gene silencing in transgenic soybean plants transformed via particle bombardment[J]. Plant Cell Report, 2003, 21(7): 676-683.
[53] El-Shemy H A, Teraishi M, Khalafalla M M, et al. Isolation of soybean plants with stable transgene expression by visual selection based on green fluorescent protein [J]. Molecular Breeding,2004, 14(3): 227-238.
[54] Furutani N, Hidaka S. Efficient production of transgenic soybean using a co-transformation method[J]. Breeding Science, 2004, 54(2): 91-98.
[55] Khalafalla M M, Rahman S M, El-Shemy H A, et al. Optimization of particle bombardment conditions by monitoring of transient sGFP (S65T) expression in transformed soybean [J]. Breeding Science, 2005, 55(3): 257-263.
[56] Kita Y, Nishizawa K, Takahashi M, et al. Genetic improvement of the somatic embryogenesis and regeneration in soybean and transformation of the improved breeding lines [J]. Plant Cell Report, 2007, 26(4): 439-447.
[57] FAO/WHO. Expert consultation on protein quality evaluation[R]. Food and Agriculture Organization of the United Nations, Rome. 1990.
[58] Young V R. Soy protein in relation to human protein and amino acid nutrition [J]. Journal of the American Dietetic Association,1991,91(7): 828-835.
[59] Dinkins R D, Reddy M S S, Meurer C A, et al. Increased sulfur amino acids in soybean plants overexpressing the maize 15 kDa zein protein [J]. In Vitro Cellular & Developmental Biology-Plant, 2001, 37(6): 742-747.
[60] Kim W S, Krishnan H B. Expression of an 11kDa 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 [J]. Plant Biotechnology Journal, 2004, 2(3): 199-210.
[61] Li Z, Meyer S, Essig J S, et al. High-level expression of maize γ-zein protein in transgenic soybean (Glycine max) [J]. Molecular Breeding, 2005, 16(1): 11-20.
[62] Kita Y, Nakamoto Y, Takahashi M, et al. Manipulation of amino acid composition in soybean seeds by the combination of deregulated tryptophan biosynthesis and storage protein deficiency[J]. Plant Cell Report, 2010, 29(1): 87-95.
[63] Falco S C, Guida T, Locke M, et al. Transgenic canola and soybean seeds with in-creased lysine [J]. Nature Biotechnology, 1995, 13: 577-582.
[64] Ishimoto M, Rahman S M, Hanafy M S, et al. Evaluation of amino acid content and nutritional quality of transgenic soybean seeds with high-level tryptophan accumulation [J]. Molecular Breeding, 2010, 25(2): 313-326.
[65] Qi Q, Huang J, Crowley J, et al. Metabolically engineered soybean seed with enhanced threonine levels: biochemical characterization and seed-specific expression of lysine-insensitive variants of aspartate kinases from the enteric bacterium Xenorhabdus bovienii [J]. Plant Biotechnology Journal, 2011, 9(2): 193-204.
[66] Cunha N B, Murad A M, Cipriano T M, et al. Waters et al. Expression of functional recombinant human growth hormone in transgenic soybean seeds [J]. Transgenic Research, 2011: 20(4): 811-826.
[67] Ding S H, Huang L Y, Wang Y D, et al. High-level expression of basic fibroblast growth factor in transgenic soybean seeds and characterization of its biological activity [J]. Biotechnology Letters, 2006, 28(12): 869-875.
[68] Piller K J, Clemente T E, Jun S M, et al. Expression and immunogenicity of an Escherichia coli K99 fimbriae subunit antigen in soybean [J]. Planta,2005, 222(1): 6-18.
[69] Nishizawa K, Kita A, Doi C, et al. Accumulation of the bioactive peptides, novokinin, LPYPR and rubiscolin, in seeds of genetically modified soybean[J]. Bioscience, Biotechnology, and Biochemistry, 2008, 72(12): 3301-3305.
[70] Tougou M, Furutani N, Yamagishi N, et al. Development of resistant transgenic soybeans with inverted repeat-coat protein genes of soybean dwarf virus [J]. Plant Cell Report,2006, 25(11): 1213-1218.
[71] Takahashi M, Uematsu Y, Kashiwaba K, et al. Accumulation of high levels of free amino acids in soybean seeds through integration of mutations conferring seed protein deficiency [J]. Planta,2003, 217(4): 577-586.
[72] TadaY, Utsumi S, Takaiwa F. Foreign gene products can be enhanced by introduction into low storage protein mutants [J]. Plant Biotechnology Journal, 2003, 1(6): 411-422.
[73] Ogawa T, Samoto M, Takahashi K. Soybean allergens and hypoallergenic soybean products [J]. Journal of Nutritional Science and Vitaminology,2000, 46(6): 271-279.
[74] Herman E M, Helm R M, Jung R, et al. Genetic modification removes an immune odominant allergen from soybean [J]. Plant Physiology, 2003, 132(1): 36-43.
[75] Lardizabal K, Effertz R, Levering C, et al. Expression of Umbelopsis ramanniana DGAT2A in seed increases oil in soybean [J]. Plant Physiology,2008, 148(1): 89-96.
[76] Rao S S, D Hildebrand. Changes in oil content of transgenic soybeans expressing the yeast SLC1 gene [J]. Lipids, 2009, 44: 945-951.
[77] Yadav N S. Genetic modification of soybean oil quality. In: Verma D.P.S. and R.C. Shoemaker (eds.) Soybean: Genetics, Molecular Biology and Biotechnology [M]. CAB INTERNATIONAL, USA, 1996:165-188.
[78] Kasai M, Kanazawa A. RNA silencing as a tool to uncover gene function and engineer novel traits in soybean [J]. Breeding Science, 2012, 61(5):468-479.
[79] Buhr T, Sato S, Ebrahim F, et al. Ribozyme termination of RNA transcripts down-regulate seed fatty acid genes in transgenic soybean [J]. The Plant Journal, 2002, 30(2): 155-163.
[80] Flores T, Karpova O, Su X, et al. Silencing of GmFAD3 gene by siRNA leads to low α-linolenic acids (18:3) of fad3-mutant phenotype in soybean [Glycine max (Merr.)] [J]. Transgenic Research, 2008, 17(5): 839-850.
[81] Li R, Yu K, Hatanaka T, et al. Vernonia DGATs increase accumulation of epoxy fatty acids in oil [J]. Plant Biotechnology Journal,2010, 8(2): 184-195.
[82] Chen R, Matsui K, Ogawa M, et al. Expression of Δ6, Δ5 desaturase and GLELO elongase genes from Mortierella alpina for production of arachidonic acid in soybean [Glycine max (L.) Merrill] seeds [J]. Plant Science, 2006, 170(2): 399-406.
[83] Eckert H, Vallee B L, Schweiger B J, et al. Co-expression of the borage Δ6 desaturase and the Arabidopsis Δ15-desaturase results in high accumulation of steridonic acid in the seeds of transgenic soybean [J]. Planta, 2006, 224(5): 1050-1057.
[84] Kajikawa M, Matsui K, Ochiai M, et al. Production of arachidonic and eicosapentaenoic acids in plants using bryophyte fatty acid Δ6-desaturase, Δ6-elongase, and Δ5-desaturase genes [J]. Bioscience, Biotechnology, and Biochemistry,2008, 72(2): 435-444.
[85] Sato S, Xing A, Ye X, et al. Production of γ-linolenic acid and stearidonic acid in seeds of marker-free transgenic soybean [J]. Crop Science, 2004, 44(2): 646-652.
[86] Bramley P M, Elmadfa I, Kafatos A, et al. Vitamin E [J]. Journal of the Science of Food and Agriculture, 2000, 80(7): 913-938.
[87] Herbers K. Vitamin production in transgenic plants [J]. Journal of Plant Physiology, 2003, 160(7): 821-829.
[88] Hoppe P P, Krennrich G. Bioavailability and potency of natural-source and all-racemic α-tocopherol in the human: a dispute [J]. European Journal of Nutrition, 2000, 39(5): 183-193.
[89] Kim Y J, Seo H Y, Park T I, et al. Enhanced biosynthesis of α-tocopherol in transgenic soybean by introducing γ-TMT gene [J]. Journal of Plant Biotechnology, 2005, 7(3): 203-209.
[90] Tavva V S, Kim Y H, Kagan I A, et al. Increased α-tocopherol content in soybean seed overexpressing the Perilla frutescens γ-tocopherol methyltrans-ferase gene [J]. Plant Cell Report, 2007, 26(1): 61-70.
[91] VanEenennaam A L, Lincoln K, Durrett T P, et al. Engineering vitamin E content: from Arabidopsis mutant to soy oil [J]. Plant Cell,2003, 15(12): 3007-3019.
[92] Ebel J. Phytoalexin synthesis: the biochemical analysis of the induction process [J]. Annual Review of Phytopathology,1986, 24: 235-264.
[93] Rivera-Vargas L I, Schmitthenner A F, Graham T L. Soybean flavonoid effects on and metabolism by Phytophthora sojae [J]. Phytochemistry, 1993, 32(4): 851-857.
[94] Subramanian S, Graham M Y, Yu O, et al. RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae [J]. Plant Physiology, 2005, 137(4): 1345-1353.
[95] VanRhijn P, Vanderleyden J. The Rhizobium-plant symbiosis [J]. Microbiology and Molecular Biology Reviews, 1995, 59(1): 124-142.
[96] Setchell K D. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones [J]. The American Journal of Clinical Nutrition, 1998, 68(6): 1333-1346.
[97] Graham T L. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates [J]. Plant Physiology, 1991, 95(2): 594-603.
[98] Yu O, Shi J, Hession A O, et al. Metabolic engineering to increase isoflavone biosynthesis in soybean seed [J]. Phytochemistry 2003, 63(7): 753-763.
[99] Zernova O V, Lygin A V, Widholm J M, et al. Modification of isoflavones in soybean seeds via expression of multiple phenolic biosynthetic genes [J]. Plant Physiology and Biochemistry, 2009, 47(9): 769-777.
[100] Kudou S, Tonomura M, Tsukamoto C, et al. Isolation and structural elucidation of the major genuine soybean saponin [J]. Bioscience, Biotechnology, and Biochemistry, 1992, 56(1): 142-143.
[101] Shiraiwa M, K. Harada K, Okubo K. Composition and structure of “group B saponin” in soybean seed [J]. Agricultural Biology and Chemistry, 1991, 55(4):911-917.
[102] Shiraiwa M, Kudo S, Shimoyamada M, et al. Composition and structure of “group A saponin” in soybean seed [J]. Agricultural Biology and Chemistry, 1991, 55(2): 315-322.
[103] Topping D L, Storer G B, Calvert G D, et al. Effect of dietary saponins on fecal bile acids and neutral sterols, plasma lipids, and lipoprotein turnover in the pig [J]. The American Journal of Clinical Nutrition, 1980, 33(4): 783-786.
[104] Ellington A A, Berhow M, Singletary K W. Induction of macroautophagy in human colon cancer cells by soybean B-group triterpenoid saponins [J]. Carcinogenesis, 2005, 26(1): 159-167.
[105] Ellington A A, Berhow M A, Singletary K W. Inhibition of Akt signaling and enhanced ERK1/2 activity and involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells [J]. Carcinogenesis, 2006, 27(2): 298-306.
[106] Takagi K, Nishizawa K, Hirose A, et al. Manipulation of saponin biosynthesis by RNA interference-mediated silencing of β-amyrin synthase gene expression in soybean [J]. Plant Cell Report, 2011, 30(10): 1835-1846.
[107] Chiera J M, Finer J J, Grabau E A. Ectopic expression of a soybean phytase in developing seeds of Glycine max to improve phosphorus availability [J]. Plant Molecular Biology, 2004, 56(6): 895-904.
[108] Nunes A C S, Vianna G R, Cuneo F, et al. RNAi-mediated silencing of the myo-inositol-1-phosphate synthase gene (GmMIPS1) in transgenic soybean inhibited seed development and reduced phytate content [J]. Planta, 2006 224(1): 125-132.
[109] Shi J, Wang H, Schellin K, et al. Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds [J]. Nature Biotechnology, 2007, 25: 930-937.
[110] Tabashnik B E. Evolution of resistance to Bacillus thuringiensis [J]. Annual Review of Entomology, 1994, 39: 47-79
[111] Owens L D, Cress D E. Genotypic variability of soybean response to Agrobacterium strains harboring the Ti or Ri plasmids [J]. Plant Physiology, 1985, 77(1): 87-94.
[112] Dufourmantel N, Tissot G, Goutorbe F, et al. Generation and analysis of soybean plastid transformants expressing Bacillus thuringiensis Cry1Ab protoxin [J]. Plant Molecular Biology, 2005, 58(5): 659-668.
[113] Miklos J A, Alibhai M F, Bledig S A, et al. Characterization of soybean exhibiting high expression of a synthetic Bacillus thuringiensis cry1A transgene that confers a high degree of resistance to lepidopteran pests [J]. Crop Science,2007, 47(1): 148-157.
[114] Walker D R, All J, McPherson R M, et al. Field evaluation of soybean engineered with a synthetic cry1Ac transgene for resistance to corn earworm, soybean looper, velvetbean caterpillar (Lepidoptera: Noctuidae), and lesser corn-stalk borer (Lepidoptera: Pyralidae) [J]. Journal of Economic Entomology,2000, 93(3): 613-622.
[115] Walker D, Boerma H R, All J, et al. Combining cry1Ac with QTL alleles from PI 229358 to improve soybean resistance to lepidopteran pests [J]. Molecular Breeding, 2002 9(1): 43-51.
[116] McLean M D, Hoover G J, Bancroft B, et al. Identification of the full-length Hs1pro-1 coding sequence and preliminary evaluation of soybean cyst nematode resistance in soybean transformed with Hs1pro-1 cDNA [J]. Canadian Journal of Botany, 2007, 85(4): 437-441.
[117] Ross J P. Effect of time and sequence of inoculation of soybeans with soybean mosaic and bean pod mottle viruses on yields and seed characters [J]. Phytopathology, 1969, 59: 1404-1408.
[118] Furutani N, Hidaka S, Kosaka Y, et al. Coat protein gene-mediated resistance to soybean mosaic virus in transgenic soybean [J]. Breeding Science, 2006, 56(2): 119-124.
[119] Wang X Y, Eggenberger A L, Forrest W, et al. Pathogen-derived transgenic resistance to soybean mosaic virus in soybean [J]. Molecular Breeding,2001, 8(2): 119-127.
[120] Di R, Purcell V, Collins G B, et al. Production of transgenic soybean lines expressing the bean pod mottle virus coat protein precursor gene [J]. Plant Cell Report, 1996, 15(10): 746-750.
[121] Reddy M S S, Ghabrial S A, Redmond C T, et al. Resistance to Bean pod mottle virus in transgenic soybean lines expressing the capsid polyprotein [J]. Phytopathology, 2001, 91(9): 831-838.
[122] Tougou M, Furutani N, Yamagishi N, et al. Development of resistant transgenic soybeans with inverted repeat-coat protein genes of soybean dwarf virus [J]. Plant Cell Report, 2006, 25(11): 1213-1218.
[123] Tougou M, Yamagishi N, Furutani N, et al. Soybean dwarf virus-resistant transgenic soybeans with the sense coat protein gene [J]. Plant Cell Report, 2007, 26(11): 1967-1975.
[124] Godoy G, Steadman J R, Dickman M B, et al. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris [J]. Physiological and Molecular Plant Pathology, 1990, 37(3): 179-191.
[125] Cunha W G, Tinoco M L P, Pancoti H L, et al. High resistance to Sclerotinia sclerotiorum in transgenic soybean plants transformed to express an oxalate decarboxylate gene [J]. Plant Pathology, 2010, 59(4): 654-660.
[126] Donaldson P A, Anderson T, Lane B G, et al. Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum [J]. Physiological and Molecular Plant Pathology, 2001, 59(6): 297-307.
[127] DeRonde J A, Laurie R N, Caetano T, et al. Comparative study between transgenic and non-transgenic soybean lines proved transgenic lines to be more drought tolerant [J]. Euphytica, 2004, 138(2): 123-132.
[128] De Ronde J A, Cress W A, Krüger G H J, et al. Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress [J]. Journal of Plant Physiology, 2004, 161(11): 1211-1224.
[129] Valente M A S, Faria J A Q A, Soares-Ramos J R L, et al. The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco [J]. The Journal of Experimental Botany, 2009, 60(2): 533-546.
[130] Vasconcelos M, Eckert H, Arahama V, et al. Molecular and phenotypic characterization of transgenic soybean expressing the Arabidopsis ferric chelate reductase gene, FRO2 [J]. Planta,2006, 224(5): 1116-1128.
[131] Padgette S R, Kolacz K H, Delannay X, et al. Development, identification, and characterization of a glyphosate-tolerant soybean line [J]. Crop Science, 1995, 35: 1451-1461.
[132] Dufourmantel N, Dubald M, Matringe M, et al. Generation and characterization of soyben and marker-free tobacco plastid transformants over-expressing a bacterial 4-hydroxyphenylpyruvate dioxygenase which provides strong herbicide tolerance [J]. Plant Biotechnology Journal, 2007, 35(5): 118-133.
[133] Kita Y, Hanafy M S, Deguchi M, et al. Generation and characterization of herbicide-resistant soybean plants expressing novel phosphinothricin N-acetyltransferase genes [J]. Breeding Science, 2009, 59(3): 245-251
[134] Rech E L, Vianna G R, Arag?o F J. High-efficiency transformation by biolistics of soybean, common bean and cotton transgenic plants [J]. Nature Protocols, 2008, 3: 410-418.
[135] Liu B, Watanabe S, Uchiyama T, et al. The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1 [J]. Plant Physiology, 2010, 153(1): 198-210.
[136] Chilton M D, Tepfer D A, Petit A, et al. Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells [J]. Nature, 1982, 295: 432-434.
[137] Kereszt A, Li D, Indrasumunar A, et al. Agrobacterium rhizogenes-mediated transformation of soybean to study root biology [J]. Nature Protocols, 2007, 2: 948-952.
[138] Indrasumunar A, Searle I, Lin M H, et al. Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr) [J]. The Plant Journal, 2011, 65(1): 39-50.
[139] Yang S M, Tang F, Gao M Q, et al. R gene-controlled host specificity in the legume-rhizobia symbiosis [J]. Proceedings of the National Academy of Sciences, 2010, 107(43): 18735-18740.
[140] Kasai M, Kanazawa A. RNA silencing as a tool to uncover gene function and engineer novel traits in soybean [J]. Breeding Science, 2012, 61(5): 468-479.
[141] Curtin S J, Zhang F, Sander J D, et al. Targeted mutagenesis of duplicated genes in soybean with zincfinger nucleases [J]. Plant Physiol., 2011, 156: 466-473.
[142] Mathieu M, Winters E K, Kong F, et al. Establishment of a soybean (Glycine max Merr. L) transposon-based mutagenesis repository [J]. Planta, 2009, 229: 279-289.