Scientia Agricultura Sinica ›› 2014, Vol. 47 ›› Issue (21): 4198-4210.doi: 10.3864/j.issn.0578-1752.2014.21.006

• EFFICIENT, SAFE AND LARGE-SCALE TRANSGENIC TECHNOLOGY: OPPORTUNITIES AND CHALLENGES • Previous Articles     Next Articles

Establishment and Prospect of Efficient Transformation Systems for Soybean

HOU Wen-sheng1, LIN Kang-xue1, CHEN Pu1, JIA Zhi-wei2, ZHOU Yang1, YU Yang1, LIU Yan-hua2   

  1. 1 Institute of Crop Science, Chinese Academy of Agricultural Sciences/National Center for Transgenic Research in Plants, Beijing 100081
    2Dabeinong Biotechnology Center, Beijing 100193
  • Received:2014-04-01 Revised:2014-06-23 Online:2014-11-01 Published:2014-11-01

Abstract: Soybean [Glycine max (L.) Merr.] is the genetically modified (GM) crops that is earliest commercially planted on large scale. GM soybean is retaining its position as the GM crop occupied the largest scale globally with food, nutritional, industrial, and pharmaceutical uses. From 1996 to 2012, total 763.1 million hectares GM soybean had been planted and by growing GM soybean, almost 37 billion US dollars income was brought to farmers. In 2013, about 84.5 million hectares of GM soybean were planted around the world in 11 countries which accounted for 48% of all the GM crops hectarage and 79% for soybean grown all over the world. Though herbicide-resistant transgenic soybean holds a leading market share in the world, soybean has been regarded as a recalcitrant crop to be transformed for many years. Efficient and stable transformation is a restrictive factor for production of transgenic soybean and gene function research. The most widely and routinely used transformation systems are cotyledonary node-Agrobacterium-mediated transformation and somatic embryo-particle-bombardment-mediated transformation. The first fertile transgenic soybean plants were produced nearly simultaneously by these two methods in 1988. Even after more than two decades, these two methods have continued to be improved and have produced most transgenic soybean plants. The transformation efficiencies of these improved protocols have been extended and the system was successfully adapted to embryogenic suspension cultures for the regeneration of fertile transgenic soybean plants. These ready systems enable us to improve agronomic characteristics or to analyze gene function in soybean by transgenic approaches. In this review, recent advances and problems in research of soybean transformation system were described, with a focus on the characteristics of soybean regeneration systems such as organogenesis, somatic embryogenesis and protoplasts system. The representative soybean transformation systems mediated by Agrobacterium tumefaciens and particle bombardment have been summarized, and described their experimental parameters such as soybean genotype, explant, regeneration system, screening system, transformation frequencies. Analysis suggests that the genotype, explant type and so on can be used in the transformation of soybean has been developed and the transformation frequencies has been improved significantly. Some reports showed higher transformation efficiency over 10% and even some over 30% in some cases. However, the date of transformation frequencies had been obtained in some research reports that involved small sample size. The transformation frequencies between different experimental replications often repeated differences greatly. Sometimes, obtained high transformation frequencies in the single factor experiment, often doesn’t get well again in multi-factor integrated experiment. It indicated that the transformation efficiency still is affected by some unknown factors that is hard to control. On the other hand, the transformation efficiency still relies on the skill of the technicians and on the tissue culture conditions of the laboratory. That leads to some problems such as the same transformation process is poor in reproducibility between laboratories, the transformation frequencies are greatly different between operators, the transformation frequencies are not stable in the same laboratory. And those problems hindered the establishment of high-throughput transformation systems for soybean. Meanwhile, the research result of soybean transformation and transgenic lines was reviewed, and the current transgenic lines for soybean breeding in China were surveyed. Further, some new genetically modified technologies used in soybean were prospected, such as genome editing techniques and precise genome modification techniques.

Key words: soybean [Glycine max (L.) Merr.], transgenic system, transformation efficiency, Agrobacterium tumefaciens, particle bombardment

[1]    James C. Global Status of Commercialized Biotech/GM Crop. International Service for the Acquisition of Agri-biotech Applications: Ithaca, NY, 2013, Brief No.46.
[2]   Ainsworth E A, Yendrek C R, Skoneczka J A, Long S P. Accelerating yield potential in soybean: Potential targets for biotechnological improvement. Plant, Cell and Environment, 2012, 35: 38-52.
[3]    Stacey G. Genetics and Genomics of Soybean. New York: Springer Science+Business Media, LLC. 2008.
[4]    中国种植业信息网. 农作物数据库. http://202.127.42.157/moazzys/ nongqing.aspx.
China Farming Information Network. Crops database. http://202.127. 42.157/moazzys/nongqing.aspx. (in Chinese)
[5]    中华人民共和国海关总署. 2013年12月全国进口重点商品量值表. http://www.customs.gov.cn/publish/portal0/tab49666/info690427.htm
General Administration of Customs of the People’s Republic of China. The national key value of goods imported in December 2013.http:// www.customs.gov.cn/publish/portal0/tab49666/info690427.htm. (in Chinese)
[6]    杨如萍, 宋雯雯, 孙石, 吴存祥, 王化俊, 韩天富. 中国不同地区科技示范县大豆单产及产量相关性状的比较. 大豆科学, 2013, 31: 557-567.
Yang R P, Song W W, Sun S, Wu C X, Wang H J, Han T F. Comparison of soybean yield and yield-related traits of agri-technology demonstration counties in different regions of China. Soybean Science, 2013, 31: 557-567. (in Chinese)
[7]    韩天富, 黄大昉. 发展我国农作物种业生物技术刻不容缓. 中国种业, 2012, 5: 1-5.
Han T F, Huang D F. Development of crop seed industry biotechnology is urgently needed in China. China Seed Industry, 2012, 5: 1-5. (in Chinese)
[8]    韩天富, 侯文胜, 王济民. 发展转基因大豆, 振兴中国大豆产业. 中国农业科技导报. 2008,10(3): 1-5.
Han T F, Hou W S, Wang J M. Developing transgenic soybean to promote soybean industry in China. Journal of Agricultural Science and Technology, 2008, 10(3): 1-5. (in Chinese)
[9]    Hinchee M A W, Connor-Ward D V, Newell C A, McDonell R E, Sato S J, Gasser C S, Fishhoff D A, Re D B, Fraley R T, Horsch R B. Production of transgenic soybean plants using Agrobacterium- mediated DNA transfer. Nature Biotechnology, 1988, 6: 915-922.
[10]   McCabe D E, Swain W F, Martinell B J, Christou P. Stable transformation of soybean (Glycine max) by particle acceleration. Nature Biotechnology, 1988, 6: 923-926.
[11]   Christou P, McCabe D E, Swain W F. Stable transformation of soybean callus by DNA-coated gold particles. Plant Physiology, 1988, 87: 671-674.
[12]   Homrich M S, Wiebke-Strohm B, Weber R L, Bodanese-Zanettini M H. Soybean genetic transformation: A valuable tool for the functional study of genes and the production of agronomically improved plants. Genetics and Molecular Biology, 2012, 35: 998-1010.
[13]   Slamet-Loedin I H, Chadha-Mohanty P, Torrizo L. Agrobacterium- mediated transformation: Rice transformation//Robert J. Henry, Agnelo Furtado. eds. Cereal Genomics: Methods and Protocols, Methods in Molecular Biology, vol. 1099. Springer Science+Business Media, New York, 2014.
[14]   Shri M, Rai A, Verma P K, Misra P, Dubey S, Kumar S, Verma S, Gautam N, Tripathi R D, Trivedi P K, Chakrabarty D. An improved Agrobacterium-mediated transformation of recalcitrant indica rice (Oryza sativa L.) cultivars. Protoplasma, 2013, 250: 631-636.
[15]   Dhir S K, Dhir S, Widholm J M. Regeneration of fertile plants from protoplasts of soybean (Glycine max L. Merr.): Genotypic differences in culture response. Plant Cell Reports, 1992, 11: 285-289.
[16]   徐香玲, 邹联沛, 刘伟华, 李集临. 向大豆导入几丁质酶基因的初步研究. 大豆科学, 1999, 18(2): 101-108.
Xu X L, Zou L P, Liu W H, Li J L. A preliminary study on transferring chitinase gene into soybeans. Soybean Science, 1999, 18(2): 101-108. (in Chinese)
[17]   Kereszt A, Li D, Indrasumunar A, Nguyen C D, Nontachaiyapoom S, Kinkema M, Gresshoff P M. Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nature Protocols, 2007, 2(4): 948-952.
[18]   Cao D, Hou W S, Song K, Sun H B, Wu C X, Gao Y S, Han T F. Assessment of conditions affecting Agrobacterium rhizogenes- mediated transformation of soybeanPlant Cell, Tissue and Organ Culture, 2009, 96: 45-52.
[19]   Cao D, Hou W S, Liu W, Yao W W, Wu C X, Liu X B, Han T F. Overexpression of TaNHX2 enhances salt tolerance of ‘composite’ and whole transgenic soybean plants. Plant Cell, Tissue and Organ Culture, 2011, 107: 541-552.
[20]   Dunwell J M, Wetten A C. Transgenic Plants: Methods and Protocols, Methods in Molecular Biology, vol. 847. Springer Science+Business Media, LLC 2012.
[21]   Somers D A, Samac D A, Olhoft P M. Recent advances in legume transformation. Plant Physiology, 2003, 131: 892-899.
[22]   Cheng T Y, Saka H, Voqui-Dinh T H. Plant regeneration from soybean cotyledonary node segments in culture. Plant Science Letters, 1980, 19: 91-99.
[23]   Barwale U B, Kerns H R, Widholm J M. Plant regeneration from callus cultures of several soybean genotypes via embryogenesis and organogenesis. Planta, 1986, 167: 473-481.
[24]   Paz M M, Martinez J C, Kalvig A B, Fonger T M, Wang K. Improved cotyledonary node method using an alter-native explant derived from mature seed for efficient Agrobacterium-mediated soybean transformation. Plant Cell Reports, 2006, 25: 206-213.
[25]   Li Z, Xing A, Moon B P, McCardell R P, Mills K, Falco S C. Site-specific integration of transgenes in soybean via recombinase- mediated DNA cassette exchange. Plant Physiology, 2009, 151: 1087-1095.
[26]   Liu H K, Yang C, Wei Z M. Efficient Agrobacterium tumefaciens- mediated transformation of soybeans using an embryonic tip regeneration system. Planta, 2004, 219: 1042-1049.
[27]   Christianson M L, Warnick D A, Carlson P S. A morpho-genetically competent soybean suspension culture. Science, 1983, 222: 632-634.
[28]   Lazzeri P A, Hildebrand D F, Collins G B. A procedure for plant regeneration from immature cotyledon tissue of soybean. Plant Molecular Biology Reporter, 1985, 3: 160-167.
[29]   Ranch J P, Oglesby L, Zielinski A C. Plant regeneration from embryo-derived tissue cultures of soybeans. In Vitro Cellular and Developmental Biology-Plant, 1985, 21: 653-658.
[30]   Finer J J, Nagasawa A. Development of an embryogenic suspension culture of soybean (Glycine max Merrill.). Plant Cell, Tissue and Organ Culture, 1988, 15: 125-136.
[31]   Finer J J, McMullen M D. Transformation of soybean via particle bombardment of embryogenic suspension culture tissue. In Vitro Cellular and Developmental Biology-Plant, 1991, 27: 175-182.
[32]   Hadi M Z, McMullen M D, Finer J J. Transformation of 12 different plasmids into soybean via particle bombardment. Plant Cell Reports, 1996,15: 500-505.
[33]   Singh R J, Klein T M, Mauvais C J, Knowlton S, Himowitz T, Kostow C M. Cytological characterization of transgenic soybean. Theoretical and Applied Genetics, 1998, 96: 319-324.
[34]   Trick H N, Dinkins R D, Santarém E R, Di R, Samoylov V, Meurer C A, Walker D R, Parrott W A, Finer J J, Collins G B. Recent advances in soybean transformation. Plant Tissue Culture Biotechnology, 1997, 3: 9-24.
[35]   Wei Z M, Xu Z H. Plant regeneration from protoplasts of soybean (Glycine max L.). Plant Cell Reports, 1988, 7: 348-351.
[36]   罗希明, 赵桂兰, 简玉瑜. 大豆原生质体的植株再生. 植物学报, 1990, 37: 616-621.
Luo X M, Zhao G L, Jian Y Y. Plant regeneration from protoplasts of soybean (Glycine max L.). Acta Botanica Sinica, 1990, 37: 616-621. (in Chinese)
[37]   Dhir S K, Dhir S, Widholm J M. Regeneration of fertile plants from protoplasts of soybean (Glycine max L. Merr.): Genotypic differences in culture response. Plant Cell Reports, 1992, 11: 285-289.
[38]   Zhang X Z, Komatsusda T. Plant regeneration from soybean (Glycine max L.) protoplasts via somatic embryogenesis. Science in China: Series B, 1993, 36: 1476-1481.
[39]   肖文言, 王连铮. 大豆原生质体培养经胚胎发生高频率再生植株. 大豆科学, 1993, 12: 249-251.
Xiao W Y, Wang L Z. Plantlet regeneration from protoplasts of soybean (Glycine max L.) through embryogenesis. Soybean Science, 1993, 12: 249-251. (in Chinese)
[40]   南相日, 刘文萍, 刘丽艳, 吕晓波, 何云霞, 卫志明. PEG介导BT基因转化大豆原生质体获转基因植株. 大豆科学, 1998, 17: 326-330.
Nan X R, Liu W P, Liu L Y, Lü X B, He Y X, Wei Z M. PEG- mediated transformation and regeneration of soybean protoplast with Bacillus Thuringiensis CrgIAc gene. Soybean Science, 1998, 17: 326-330. (in Chinese)
[41]   Dhir S K, Dhir S, Savka M A, Belanger F, Kriz A L, Farrand S K, Widholm J M. Regeneration of transgenic soybean (Glycine max) plants from electroporated protoplasts. Plant Physiology, 1992, 99: 81-88.
[42]   Hansen G, Wright M S. Recent advances in the transformation of plants. Trends in Plant Science, 1999, 4: 226-231.
[43]   Yamada T, Takagi K, Ishimoto M. Recent advances in soybean transformation and their application to molecular breeding and genomic analysis. Breeding Science, 2012, 61: 480-494.
[44] Zhang A Y, Xing A Q, Staswick P, Clemente T A. The use of glufosinate as a selective agent in Agrpbacterium-mediated transformation of soybean. Plant Cell Tissue and Organ Culture, 1999, 56: 37-46.
[45]   Donaldson P A, Simmonds D H. Susceptibility to Agrobacterium tumefaciens and cotyledonary node transformation in short-season soybean. Plant Cell Reports, 2000, 19: 478-484.
[46]   Clemente T E, LaVallee B J, Howe A R, Conner-Wardb D, Rozmanb R J, Hunterb P E, Broylesb D L, Kastenb D S, Hincheeb M A. Progeny analysis of glyphosate selected transgenic soybean derived from Agrpbacterium-mediated transformation. Crop Science, 2000, 40: 797-803.
[47]   Olhoft P M, Flagel L E, Donovan C M, Somers D A. Efficient soybean transformation using hygromycin B selection in the cotyledonary- node method. Planta, 2003, 216: 723-735.
[48]   Zeng P, Vadnais D A, Zhang Z, Polacco J C. Refined glufosinate selection in Agrobacterium-mediated transformation of soybean [Glycine max (L.) Merrill]. Plant Cell Reports, 2004, 22: 478-482.
[49]   Paz M M, Shou H, Guo Z, Zhang Z, Banerjee A K, Wang K. Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explant. Euphytica, 2004, 36: 167-179.
[50]   Xue R G, Xie H F, Zhang B. A multi-needle-assisted transformation of soybean cotyledonary node cells. Biotechnology Letters2006, 28: 1551-1557.,
[51]   Yi X P, Yu D Y. Transformation of multiple soybean cultivation and selection parameters on Agrobacterium tumefaciens. African Journal of Biotechnology, 2006, 5: 1989-1993.
[52]   Liu S J, Wei Z M, Huang J Q. The effect of co-cultivation and selection parameters on Agrobacterium-mediated transformation of Chinese soybean varieties. Plant Cell Reports2008, 27: 489-498.,
[53]   Paz M M, Martinez J C, Kalvig A B, Fonger T M, Wang K. Improved cotyledonary node method using an alternative explant derived from mature seed for efficient Agrobacterium-mediated soybean transformation. Plant Cell Reports, 2006, 25: 206-213.
[54]   Zia M, Mirza B, Malik S A, Chaudhary M F. Expression of rol genes in transgenic soybean (Glycine max L.) leads to changes in plant phenotype, leaf morphology, and flowering time. Plant Cell, Tissue Organ Culture, 2010, 103: 227-236.
[55]   Liu H K, Yang C, Wei Z M. Efficient Agrobacterium tumefaciens- mediated transformation of soybeans using an embryonic tip regeneration system. Planta, 2004, 219: 1042-1049.
[56]   Dang W, Wei Z. An optimized Agrobacterium-mediated transformation for soybean for expression of binary insect resistance genes. Plant Science2007, 173: 381-389.,
[57]   Khan R. Method of transforming soybean. US Patents, US 2004/0034889 A1. 2004-2-19.
[58]   Wang G L, Xu Y N. Hypocotyl-based Agrobacterium-mediated transformation of soybean (Glycine max) and application for RNA interference. Plant Cell Reports, 2008, 27: 1177-1184.
[59]   Dan Y, Armstrong C L, Dong J, Feng X R, Fry J E, Keithly G E, Martinell B J, Roberts G A, Smith L A, Tan L J, Duncan D R. Lipoic acid-a unique olant transformation enhancer. In Vitro Celluar & Deverlopmental Biology-Plant, 2009, 45: 630-638.
[60]   Martinell B J, Julson L S, Emler C A, Huang Y, McCabe D E, Williams E J. Soybean transformation method. US Patents, US 8030076 B2. 2011-10-4.
[61]   Hong H P, Zhang H Y, Olhoft P, Hill S, Wiley H, Toren E, lebrand H H, Jones T, Cheng M. Organogeniccallusas the target for plant regeneration and transformation via Agrobacterium in soybean (Glycine max(L.) Merr.). In Vitro Celluar & Deverlopmental Biology- Plant, 2007, 43: 558-568.
[62]   Hwang Y, Dawson J, Sigareva M, Que Q D. Transformation of immature soybean seeds through organogenesis. US Patents, US 2008/0229447 A1. 2008-9-18.
[63]   Zhang H, Que Q. Method for transforming soybean (Glycine max). US Patents, US 2009/0023212 A1. 2009-1-22.
[64] Yan B, Reddy M S S, Collins G B, Dinkins R D. Agrobacterium tumefaciens-mediated transformation of soybean [Glycine max (L.) Merrill.] using immature zygotic cotyledon explants. Plant Cell Reports, 2000, 19: 1090-1097.
[65]   Ko T S, Lee S, Krasnyanski S, Korban S S. Two critical factora are reqyired for efficient transformation of multiple soybean cultivars: Agrobacterium strain and orientation of immature cotyledonary explant. Theoretical and Applied Genetics, 2003, 107: 439-447.
[66]   Newell C A. Plant transformation technology. Developments and applications. Molecular Biotecjnology, 2000, 16: 53-65.
[67]   Aragão F J L, Sarokin L, Vianna G R, Rech E L. 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. Theoretical and Applied Genetics, 2000, 101: 1-6.
[68]   Finer J J, Vain P, Jones M W, McMullen M D. Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Reports1992, 11: 323-328.,
[69]   Sato S, Newell C, Kolacz K, Tredo L, Finer J, Hinchee M. Stable transformation via particle bombardment in two different soybean regeneration systems. Plant Cell Reports1993, 12: 408-413.,
[70]   Khalafalla M M, Rahman S M, El-Shemy H A, Nakamoto Y, Wakasa K, Ishimoto M. Optimization of particle bombardment conditions by monitoring of transient sGFP (S65T) expression in transformed soybean. Breed Science2005, 55: 257-263.,
[71]   Vianna G R, Aragäo F J, Rech E L. A minimal DNA cassette as a vector for gemetic transformation of soybean (Glycine max). Genetics and Molecular Research, 2011, 10: 382-390.
[72]   Meurer C A, Dinkins R D, Redmond C T, McAllister K P, Tucker D T, Walker D R, Parrott W A, Trick H N, Essig J S, Frantz H M, Finer J J, Collins G B. Embryogenic response of multiple soybean [Glycine max (L.) Merrill] cultivars across three locations. In Vitro Celluar & Deverlopmental Biology-Plant, 2001, 37: 62-67.
[73]   Tomlin E S, Branch S R, Chamberlain D, Gabe H, Wright M S, Stewart C N. Screening of soybean, Glycine max (L.) Merrill, lines for somatic embryo induction and maturation capability from immature cotyledons. In Vitro Celluar & Deverlopmental Biology-Plant, 2002, 38: 543-548.
[74]   Nishizawa K, Kita Y, Kitayama M, Ishimoto M. A red fluorescent protein, DsRed2, as a visual reporter for transient expression and stable transformation in soybean. Plant Cell Reports2006, 25: 1355-1361.,
[75]   Kita Y, Nishizawa K, Takahashi M, Kitayama M, Ishimoto M. Genetic improvement of the somatic embryogenesis and regeneration in soybean and transformation of the improved breeding lines. Plant Cell Reports2007, 26: 439-447.,
[76]   Kita Y, Nakamoto Y, Takahashi M, Kitamura K, Wakasa K, Ishimoto M. Manipulation of amino acid composition in soybean seeds by the combination of deregulated tryptophan biosynthesis and storage protein deficiency. Plant Cell Reports2010, 29: 87-95.,
[77]   Maughan P J, Philip R, Cho M J, Widholm J M, Vodkin L O. Biolistic transformation, expression, and inheritance of bovine β-casein in soybean (Glycine max). In Vitro Celluar & Deverlopmental Biology-Plant, 1999, 35: 344-349.
[78]   Stewart C N J, Adang M J, All J N, Boerma H R, Cardineau G, Tucker  D, Parrott W A. Genetic transformation, recovery, and characterization of fertile soybean transgenic for a synthetic Bacillus thuringiensiscryIAc gene. Plant Physiology1996, 112: 121-129.,
[79]   Reddy M S S, Ghabrial S A, Redmond C T, Dinkins R D, Collins G B. Resistance to Bean pod mottle virus Phytopathology2001, 91: 831-838., in transgenic soybean lines expressing the capsid polyprotein.
[80]   Herman E M, Helm R M, Jung R, Kinney A J. Genetic modification removes an immunodominant allergen from soybean. Plant Physiology2003, 132: 36-43.,
[81]   刘伯林, 岳绍先, 胡乃璧, 李小兵, 翟文学, 李诺, 朱荣焕, 朱立, 毛大璋, 周佩珍. 龙葵阿特拉津抗性基因向大豆叶绿体基因组的转移及在转基因植株中的表达. 科学通报, 1988, 19: 1519-1520.
Liu B L, Yue S X, Hu N B, Li X B, Zhai W X, Li N, Zhu R H, Zhu L H, Mao D Z, Zhou P Y. Transferring of morel anti-Atrazene gene into soybean chloroplast genome and its expression in transgenic plants. Chinese Science Bulletin, 1988, 19: 1519-1520. (in Chinese)
[82]   刘博林, 岳绍先, 胡乃璧, 李小兵, 翟文学, 李诺, 朱荣焕, 朱立煌, 毛大璋, 周佩珍. 龙葵Atrazine抗性基因向大豆叶绿体的转移及在转基因植株中的表达. 中国科学: B, 1989, 7: 699-705.
Liu B L, Yue S X, Hu N B, Li X B, Zhai W X, Li N, Zhu R H, Zhu L H, Mao D Z, Zhou P Y. Transferring of morel anti-Atrazene gene into soybean chloroplast and its expression in transgenic plants. Science in China: SeriesB, 1989, 7: 699-705. (in Chinese)
[83]   岳绍先, 刘博林, 毛大璋, 李小兵, 胡乃壁, 傅骏华, 李连城, 朱立煌. 抗阿特拉津转基因大豆植株后代的遗传分析. 植物学报, 1990, 32: 343-349.
Yue S X, Liu B L, Mao D Z, Li X B, Hu N B, Fu J H, Li L C, Zhu L H. A genetic analysis to the progenies of atrazine-resistance transgenic soybean plant. Acta Botanica Sinica, 1990, 32: 343-349. (in Chinese)
[84]   傅骏骅, 李连城, 苑红丽, 岳绍先, 朱立煌. 抗阿特拉津(Atrazine)转基因大豆植株的田间检测表现. 作物学报, 1993, 19: 497-500.
Fu J H, Li L C, Yuan H L, Yue S X, Zhu L H. Expression of the Atrazine-resistant transgenic soybean plants in field test. Acta Agronomica Sinica, 1993, 19: 497-500. (in Chinese)
[85]   岳绍先, 傅骏骅, 李连城, 苑红丽. 抗atrazine转基因大豆的抗性遗传及某些生理、农艺性状. 植物生理学报, 1996, 22: 385-391.
Yue S X, Fu J H, Li L C, Yuan H L.The resistance inheritance and some physiological and agronomic traits of transgenic soybean plants with Atrazine-resistance gene. Acta Phytophysiologica Sinca, 1996, 22: 385-391. (in Chinese)
[86]   Sun H B, Jia Z, Cao D, Jiang B, Wu C X, Hou W S, Liu Y K, Fei Z H, Zhao D Z, Han T F. GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PLoS One, 2011, 6: e29238.
[87]   Song S K, Hou W S, Godo I, Wu C X, Yu Y, Matityahu I, Hacham Y, Sun S, Han T F, Amir R. Soybean seeds expressing feedback- insensitive cystathionine 1 γ-synthase exhibit higher content of methionine. Journal of Experimental Botany, 2013, 64: 1917-1926.
[88]   Wang X R, Wang Y X, Tian J, Lim B L, Yan X L, Liao H. Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiology, 2009, 151: 233-240.
[89]   Zhou J, Xie J N, Liao H, Wang X R. Overexpression of β-expansin gene GmEXPB2 improves phosphorus efficiency in soybean. Physiologia Plantarum, 2014, 150: 194-204.
[90]   Suo H C, Ma Q B, Ye K X, Yang C Y, Tang Y J, Hao J, Zhang Z Y, Chen M L, Feng Y Q, Nian H. Overexpression of AtDREB1A causes a severe dwarf phenotype by decreasing endogenous gibberellin levels in soybean [ Glycine max (L.) Merr.]. PLoS One, 2012, 7: e45568.
[91]   Zhang X X, Tang Y J, Ma Q B, Yang C Y, Mu Y H, Suo H C, Luo L H, Nian H. OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean. PLoS One, 2013, 8: e83011.
[92]   Liu M, Li D M, Wang Z K, Meng F L, Li Y G, Wu X X, Teng W L, Han Y P, Li W B. Transgenic expression of ThIPK2 gene in soybean improves stress tolerance, oleic acid content and seed size. Plant Cell, Tissue and Organ Culture, 2012, 111: 277-289.
[93]   Li Y J, Zhang J C, Zhang J, Hao L, Hua J P, Duan L S, Zhang M C, Li Z H. Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions. Plant Biotechnology Journal, 2013, 11: 747-758.
[94] Chen D F, Zhang M, Wang Y Q, Chen X W. Expression of γ-tocopherol methyltransferase gene from Brassica napus increased α-tocopherol content in soybean seed. Biologia Plantarum, 2012, 56: 131-134.
[95]   Esvelt K M, Wang H H. Genome-scale engineering for systems and synthetic biology. Molecular Systems Biology, 2013, 9: 641.
[96]   , 张毅, 陈坤玲, 单奇伟, 王延鹏, 梁振, 高彩霞. CRISPR/Cas系统: RNA靶向的基因组定向编辑新技术. 遗传, 2013, 35(11): 1-9.
Li J, Zhang Y, Chen K L, Shan Q W, Wang Y P, Liang Z, Gao C X. CRISPR/Cas: A novel way of RNA-guided genome editing. Heredits, 2013, 35(11): 1-9. (in Chinese)
[97]   Bibikova M, Beumer K, Trautman J K, Carroll D. Enhancing gene targeting with designed zinc finger nucleases. Science, 2003, 300: 764.
[98]   Shan Q W, Wang Y P, Chen K L, Liang Z, Li J, Zhang Y, Zhang K, Liu J X, Voytas D F, Zheng X L, Zhang Y, Gao C X. Rapid and efficient gene modification in rice and Brachypodium using TALENs. Molecular Plant, 2013, 6: 1365-1368.
[99]   Shan Q W, Wang Y P, Li J, Zhang T, Chen K L, Liang Z, Zhang K, Liu J X, Xi J J, Qiu J L, Gao C X. Targeted genome modification of crop plants using a CRISPR/Cas system. Nature Biotechnology, 2013, 31: 686-688.
[100] Feng Z Y, Zhang B T, Ding W N, Liu X D, Yang D L, Wei P L, Cao F Q, Zhu S H, Zhang F, Mao Y F, Zhu J K. Efficient genome editing in plants using a CRISPR/Cas system. Cell Research, 2013, 23: 1229-1232.
[101] Cong L, Ran F A, Cox D, Lin S L, Barretto R, Habib N, Hsu P D, Wu X B, Jiang W Y, Marraffini L A, Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339: 819-823.
[102] Luo K, Duan H, Zhao D, Zheng X, Deng W, Chen Y, Stewart C N Jr, McAvoy R, Jiang X, Wu Y, He A, Pei Y, Li Y. ‘GM-gene-deletor’: fused loxP-FRT recognition sequences dramatically improve the efficiency of FLP or CRE recombinase on transgene excision from pollen and seed of tobacco plants. Plant Biotechnology Journal, 2007, 5: 263-274.
[103] Ow D W. Recombinase-mediated gene stacking as a transformation operating system. Journal of Integrative Plant Biology, 2011, 53: 512-519.
[104] Tzfira T, Frankman L R, Vaidya M, Citovsky V. Site-specific integration of Agrobacterium tumefaciens T-DNA via double-stranded intermediates. Plant Physiology, 2003, 133: 1011-1023.
[105] Shukla V K, Doyon Y, Miller J C, DeKelver R C, Moehle E A, Worden S E, Mitchell J C, Arnold N L, Gopalan S, Meng X, Choi V M, Rock J M, Wu Y Y, Katibah G E, Zhifang G, McCaskill D, Simpson M A, Blakeslee B, Greenwalt S A, Butler H J, Hinkley S J, Zhang L, Rebar E J, Gregory P D, Urnov F D. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature, 2009, 459: 437-441.
[1] LI YiLing,PENG XiHong,CHEN Ping,DU Qing,REN JunBo,YANG XueLi,LEI Lu,YONG TaiWen,YANG WenYu. Effects of Reducing Nitrogen Application on Leaf Stay-Green, Photosynthetic Characteristics and System Yield in Maize-Soybean Relay Strip Intercropping [J]. Scientia Agricultura Sinica, 2022, 55(9): 1749-1762.
[2] JIANG FenFen, SUN Lei, LIU FangDong, WANG WuBin, XING GuangNan, ZHANG JiaoPing, ZHANG FengKai, LI Ning, LI Yan, HE JianBo, GAI JunYi. Geographic Differentiation and Evolution of Photo-Thermal Comprehensive Responses of Growth-Periods in Global Soybeans [J]. Scientia Agricultura Sinica, 2022, 55(3): 451-466.
[3] YAN Qiang,XUE Dong,HU YaQun,ZHOU YanYan,WEI YaWen,YUAN XingXing,CHEN Xin. Identification of the Root-Specific Soybean GmPR1-9 Promoter and Application in Phytophthora Root-Rot Resistance [J]. Scientia Agricultura Sinica, 2022, 55(20): 3885-3896.
[4] ZHAO DingLing,WANG MengXuan,SUN TianJie,SU WeiHua,ZHAO ZhiHua,XIAO FuMing,ZHAO QingSong,YAN Long,ZHANG Jie,WANG DongMei. Cloning of the Soybean Single Zinc Finger Protein Gene GmSZFP and Its Functional Analysis in SMV-Host Interactions [J]. Scientia Agricultura Sinica, 2022, 55(14): 2685-2695.
[5] REN JunBo,YANG XueLi,CHEN Ping,DU Qing,PENG XiHong,ZHENG BenChuan,YONG TaiWen,YANG WenYu. Effects of Interspecific Distances on Soil Physicochemical Properties and Root Spatial Distribution of Maize-Soybean Relay Strip Intercropping System [J]. Scientia Agricultura Sinica, 2022, 55(10): 1903-1916.
[6] ZHAO DeQiang,LI Tong,HOU YuTing,YUAN JinChuan,LIAO YunCheng. Benefits and Marginal Effect of Dry Matter Accumulation and Yield in Maize and Soybean Intercropping Patterns [J]. Scientia Agricultura Sinica, 2020, 53(10): 1971-1985.
[7] PANG Ting,CHEN Ping,YUAN XiaoTing,LEI Lu,DU Qing,FU ZhiDan,ZHANG XiaoNa,ZHOU Ying,REN JianRui,WANG Tian,WANG Jin,YANG WenYu,YONG TaiWen. Effects of Row Spacing on Dry Matter Accumulation, Grain Filling and Yield Formation of Different Nodulation Characteristic Soybeans in Intercropping [J]. Scientia Agricultura Sinica, 2019, 52(21): 3751-3762.
[8] LIAN Yun,LI HaiChao,LI JinYing,WANG JinShe,WEI He,LEI ChenFang,WU YongKang,LU WeiGuo. Distribution of Soybean Cyst Nematode Resistance Allele Rhg1 and Rhg4 in Huang-Huai Soybean Varieties [J]. Scientia Agricultura Sinica, 2019, 52(15): 2559-2566.
[9] NIU Lu, ZHAO QianQian, YANG Jing, XING GuoJie, ZHANG Wei, HE HongLi, YANG XiangDong. Over-Expression of Yeast PAC1 Confers Enhanced Resistance to Soybean mosaic virus in Transgenic Soybean [J]. Scientia Agricultura Sinica, 2018, 51(2): 217-225.
[10] WANG DaGang, LI Kai, ZHI HaiJian. Progresses of Resistance on Soybean Mosaic Virus in Soybean [J]. Scientia Agricultura Sinica, 2018, 51(16): 3040-3059.
[11] ZHOU Li, FU ZhiDan, DU Qing, CHEN Ping, YANG WenYu, YONG TaiWen. Effects of Reduced N Fertilization on Crop N Uptake, Soil Ammonia Oxidation and Denitrification Bacteria Diversity in Maize/Soybean Relay Strip Intercropping System [J]. Scientia Agricultura Sinica, 2017, 50(6): 1076-1087.
[12] SHEN Jian-guo, GAO Fang-luan, CAI Wei, JIN Jing, LIAO Fu-rong, WU Zu-jian. Multiplex RT-PCR for Simultaneous Detection of Bean pod mottle virus and Soybean mosaic virus in Imported Soybean Seeds [J]. Scientia Agricultura Sinica, 2016, 49(4): 667-676.
[13] YANG Yu-juan, YAO Yi-sha, QIN Yu-chang, QIU Jing, LI Jun-guo, LI Jun, GU Xu. Investigation and Analysis of Main AFN in Soybean Meal and Fermented Soybean Meal [J]. Scientia Agricultura Sinica, 2016, 49(3): 573-580.
[14] LIU Xiao-bin, LIU Na, LI Fu-kuan, WU Li-zhu, ZHANG Jie, WANG Dong-mei. Establishment of TRV-mediated Transient Gene-Silencing System in Soybean [J]. Scientia Agricultura Sinica, 2015, 48(12): 2479-2486.
[15] XIANG Shi-hua, WANG Wu-bin, HE Qing-yuan, YANG Hong-yan, LIU Cheng, XING Guang-nan, ZHAO Tuan-jie, GAI Jun-yi. Identification of QTL/Segments Related to Agronomic Traits Using CSSL Population Under Multiple Environments [J]. Scientia Agricultura Sinica, 2015, 48(1): 10-22.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!