Advertisement

Improved Agrobacterium tumefaciens-mediated transformation of soybean [Glycine max (L.) Merr.] following optimization of culture conditions and mechanical techniques

  • Alkesh Hada
  • Veda Krishnan
  • M. S. Mohamed Jaabir
  • Archana Kumari
  • Monica Jolly
  • Shelly Praveen
  • Archana Sachdev
Plant Tissue Culture
  • 21 Downloads

Abstract

In the present study, Agrobacterium tumefaciens-mediated transformation of Glycine max (L.) Merr. (soybean) cv. DS-9712 using half-seed explants was optimized for eight different parameters, including seed imbibition, medium pH, infection mode (sonication and vacuum infiltration), co-cultivation conditions, concentrations of supplementary compounds, and selection. Using this improved protocol, maximum transformation of 14% and regeneration efficiencies of 45% were achieved by using explants prepared from mature seeds imbibed for 36 h, infected with A. tumefaciens strain EHA105 at an optical density (OD600) of 0.8, suspended in pH 5.4 medium containing 0.2 mM acetosyringone and 450 mg L−1 L-cysteine, followed by sonication for 10 s, vacuum infiltration for 2 min, and co-cultivated for 3 d on 35 mg L−1 kanamycin-containing medium. Independent transgenic lines were confirmed to be transgenic after ß-glucuronidase histochemical assays, polymerase chain reaction, and southern hybridization analysis. The protocol developed in the present study showed high regeneration efficiency within a relatively short time of 76 d. This rapid and efficient protocol might overcome some hurdles associated with the genetic manipulation of soybean.

Keywords

Agrobacterium tumefaciens Half-seed explants Soybean transformation Regeneration 

Notes

Acknowledgements

The authors are very grateful to Dr. Andy Ganapathi (Vice Chancellor, Bharathiar University, Coimbatore, India) for his valuable guidance in improving soybean transformation.

Author contributions

AS conceived and designed the experiments. AH and VK performed the experiments and compiled and analyzed the data. AK, MJ, and AH generated the pictures. AH, VK, and AS prepared the manuscript. SP and MSMJ helped in manuscript revision. All authors read and approved the final manuscript.

Funding

This work was supported by National Agriculture Science Fund (NASF) program by the Indian Council of Agricultural Research (ICAR), India.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11627_2018_9944_MOESM1_ESM.docx (233 kb)
ESM 1 (DOCX 232 kb)

References

  1. Acereto-Escoffie POM, Chi-Manzanero BH, Echeverria-Echeverria S, Grijalva R, Kay AJ, González-Estrada T, Castaño E, Rodriguez-Zapata LC (2005) Agrobacterium-mediated transformation of Musa acuminata cv “grand nain” scalps by vacuum infiltration. Sci Hortic 105:359–371CrossRefGoogle Scholar
  2. Amoah BK, Wu H, Sparks C, Jones HD (2001) Factors influencing Agrobacterium-mediated transient expression of uidA in wheat inflorescence tissue. J Exp Biol 52:1135–1142Google Scholar
  3. An X, Wang B, Liu L, Jiang H, Chen J, Ye S, Chen L, Guo P, Huang X, Peng D (2014) Agrobacterium-mediated genetic transformation and regeneration of transgenic plants using leaf midribs as explants in ramie [Boehmerianivea (L.) gaud]. Mol Biol Rep 41:3257–3269PubMedCrossRefPubMedCentralGoogle Scholar
  4. Ananthakrishnan G, Xia X, Amutha S, Singer S, Muruganantham M, Yablonsky S, Fischer E, Gaba V (2007) Ultrasonic treatment stimulates multiple shoot regeneration and explant enlargement in recalcitrant squash cotyledon explants in vitro. Plant Cell Rep 26:267–276PubMedCrossRefPubMedCentralGoogle Scholar
  5. Arun M, Subramanyam K, Theboral J, Ganapathi A, Manickavasagam M (2014) Optimized shoot regeneration for Indian soybean: the influence of exogenous polyamines. Plant Cell Tissue Organ Cult 117:305–309CrossRefGoogle Scholar
  6. Bakshi S, Sadhukhan A, Mishra S, Sahoo L (2011) Improved Agrobacterium-mediated transformation of cowpea via sonication and vacuum infiltration. Plant Cell Rep 30:2281–2292PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bechtold N, Pelletier G (1995) In-planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–326Google Scholar
  8. Beranová M, Rakouský S, Vávrová Z, Skalický T (2008) Sonication assisted Agrobacterium- mediated transformation enhances the transformation efficiency in flax (Linum usitatissimum L.). Plant Cell Tissue Organ Cult 94:253–259CrossRefGoogle Scholar
  9. Bolton GW, Nester EW, Gordon MP (1986) Plant phenolic compounds induce expression of the Agrobacterium tumefaciens loci needed for virulence. Science 232:983–985PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bowen BA (1993) Markers for gene transfer. In: Kung S, Wu R (eds) Transgenic Plants: Engineering and Utilization, Academic Press, New York pp 89–123Google Scholar
  11. Canche-Moo RLR, Ku-Gonzalez A, Burgeff C, Loyola-Vargas VM, Rodrı’guez-Zapata LC, Castan’o E (2006) Genetic transformation of Coffea canephora by vacuum infiltration. Plant Cell Tissue Organ Cult 84:373–377CrossRefGoogle Scholar
  12. Chakrabarty R, Viswakarma N, Bhat SR, Kirti PB, Singh BD, Chopra VL (2002) Agrobacterium-mediated transformation of cauliflower: optimization of protocol and development of Bt-transgenic cauliflower. J Biosci 27:495–502PubMedCrossRefPubMedCentralGoogle Scholar
  13. Charity JA, Holland L, Donaldson SS, Grace L, Walter C (2002) Agrobacterium-mediated transformation of Pinus radiata organogenic tissue using vacuum-infiltration. Plant Cell Tissue Organ Cult 70:51–60CrossRefGoogle Scholar
  14. Cheng M, Fry JE, Pang S, Zhou H, Hironaka CM, Duncan DR, Connor TW, Wan Y (1997) Genetic transformation of wheat mediated by Agrobacterium tumefaciens. Plant Physiol 115:971–980PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cho HJ, Farrand SK, Noel GR, Widholm JM (2000) High efficiency induction of soybean hairy roots and propagation of the soybean cyst nematode. Planta 210:195–204PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chopra R, Saini R (2012) Use of sonication and vacuum infiltration for Agrobacterium-mediated transformation of an Indian lentil (Lens culinaris Medik.) cultivar. Sci Hortic 143:127–134CrossRefGoogle Scholar
  17. Clemente TE, LaVallee BJ, Howe AR, Conner-Ward D, Rozman RJ, Hunter PE, Broyles DL, Kasten DS, Hinchee MA (2000) Progeny analysis of glyphosate selected transgenic soybean derived from Agrobacterium-mediated transformation. Crop Sci 40:797–803CrossRefGoogle Scholar
  18. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dan Y (2008) Biological functions of antioxidants in plant transformation. In Vitro Cell Dev Biol-Plant 44:149–161CrossRefGoogle Scholar
  20. Das DK, Reddy MK, Upadhyaya KC, Sopory SK (2002) An efficient leaf-disk culture method for the regeneration via somatic embryogenesis and transformation of grape (Vitis vinifera L.). Plant Cell Rep 20:999–1005CrossRefGoogle Scholar
  21. Di R, Purcell V, Collins GB, Ghabrial SA (1996) Production of transgenic soybean line expressing the bean pod mottle virus coat protein precursor gene. Plant Cell Rep 15:746–750PubMedCrossRefPubMedCentralGoogle Scholar
  22. Dong J, Kharb P, Teng W, Hall TC (2001) Characterization of rice transformed via an Agrobacterium inflorescence approach. Mol Breeding 7:187–194CrossRefGoogle Scholar
  23. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  24. Duque AS, Araujo SS, Cordeiro MA, Santos DM, Fevereiro MP (2007) Use of fused gfp and gus reporters for the recovery of transformed Medicago truncatula somatic embryos without selective pressure. Plant Cell Tissue Organ Cult 90:325–330CrossRefGoogle Scholar
  25. Enríquez-Obregón GA, Vázquez-Padrón RI, Prieto-Samsonov DL, De la Riva GA, Selman-Housein G (1998) Herbicide-resistant sugarcane (Saccharum officinarum L.) plants by Agrobacterium-mediated transformation. Planta 206:20–27CrossRefGoogle Scholar
  26. Franklin G, Carpenter L, Davis E, Reddy CS, Al-Abed D, Alaiwi WA, Parani M, Smith B, Sairam RV (2004) Factors influencing regeneration of soybean from mature and immature cotyledons. Plant Growth Regul 43:73–79CrossRefGoogle Scholar
  27. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–115PubMedCrossRefPubMedCentralGoogle Scholar
  28. Gnasekaran P, Antony JJJ, Uddain J, Subramaniam S (2014) Agrobacterium-mediated transformation of the recalcitrant Vanda Kasem’s delight orchid with higher efficiency. Sci World J 2014:583934CrossRefGoogle Scholar
  29. Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research, 2nd edn. John Wiley and Sons, New YorkGoogle Scholar
  30. Goodman RN, Novacky AJ (1994) The hypersensitive reaction in plants to pathogens. A resistant phenomenon. APS PRESS, St. Paul, MinnesotaGoogle Scholar
  31. Guivarch A, Caissard J, Brown S, Marie D, Dewitte W, Vanonckelen H, Chriqui D (1993) Localization of target cells and improvement of Agrobacterium-mediated transformation efficiency by direct acetosyringone pretreatment of carrot root disks. Protoplasma 174:10–18CrossRefGoogle Scholar
  32. Gupta S, Gupta S, Bhat V, Gupta MG (2006) Somatic embryogenesis and Agrobacterium-mediated genetic transformation in Indian accessions of Lucerne (Medicago sativa L.). Ind J Biotechnol 5:269–275Google Scholar
  33. Hada A, Krishnan V, Punjabi M, Basak N, Pandey V, Jeevaraj T, Marathe A, Gupta AK, Jolly M, Kumar A, Dahuja A, Manickavasagam M, Ganapathi A, Sachdev A (2016) Refined glufosinate selection and its extent of exposure for improving the Agrobacterium-mediated transformation in Indian soybean (Glycine max) genotype JS-335. Plant Biotechnol 33:341–350CrossRefGoogle Scholar
  34. Hansen G (2000) Evidence for Agrobacterium-induced apoptosis in maize cells. Mol Plant-Microbe Interact 13:649–657PubMedCrossRefPubMedCentralGoogle Scholar
  35. Hardegger M, Sturm A (1998) Transformation and regeneration of carrot (Daucus carota L.). Mol Breeding 4:119–127CrossRefGoogle Scholar
  36. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hinchee MAW, Conor-Ward DV, Newell CA, McDonnell RE, Sato SJ, Gasser CS, Fischhoff DA, Re DB, Fraley RT, Horsch RB (1988) Production of transgenic soybean plants using Agrobacterium-mediated DNA transfer. Nat Biotechnol 6:915–922CrossRefGoogle Scholar
  38. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218CrossRefGoogle Scholar
  39. Indurker S, Misra HS, Eapen S (2010) Agrobacterium-mediated transformation in chickpea (Cicer arietinum L.) with an insecticidal protein gene: optimization of different factors. Physiol Mol Biol Plants 16:273–284PubMedPubMedCentralCrossRefGoogle Scholar
  40. Ismael KA, Antar EN (2014) Establishment of high-efficiency Agrobacterium-mediated transformation conditions of soybean callus. Ind J Biotechnol 13:459–463Google Scholar
  41. Jaiwal PK, Kumari R, Ignacimuthu S, Potrykus I, Sautter C (2001) Agrobacterium tumefaciens-mediated transformation of mungbean (Vigna radiata) a recalcitrant grain legume. Plant Sci 161:239–247PubMedCrossRefGoogle Scholar
  42. James D, Uratsu S, Cheng J, Negri P, Viss P, Dandekar A (1993) Acetosyringone and osmo-protectants like betaine or proline synergically enhance Agrobacterium-mediated transformation of apple. Plant Cell Rep 12:559–563PubMedCrossRefGoogle Scholar
  43. Jefferson RA, Kavanagh TA, Bevan MW (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol 5:387–405CrossRefGoogle Scholar
  44. Joao L, Brown A (1993) Enhanced transformation of tomato co-cultivated with Agrobacterium tumefaciens C58 CIRIF- R PGSFRI161 in the presence of acetosyringone. Plant Cell Rep 12:422–425Google Scholar
  45. Joersbo M, Brunstedt J (1990) Direct gene transfer to plant protoplast by mild sonication. Plant Cell Rep 9:207–210PubMedCrossRefGoogle Scholar
  46. Joersbo M, Brunstedt J (1992) Sonication: a new method for gene transfer to plants. Physiol Plant 85:230–234CrossRefGoogle Scholar
  47. Khan MR, Rashid H, Ansar M, Chaudury Z (2003) High frequency shoot regeneration and Agrobacterium-mediated DNA transfer in canola (Brassica napus). Plant Cell Tissue Organ Cult 75:223–231CrossRefGoogle Scholar
  48. Kim JH, Lamotte CE, Hack E (1990) Plant regeneration in vitro from primary leaf nodes of soybean (Glycine max) seedlings. J Plant Physiol 136:664–669CrossRefGoogle Scholar
  49. Ko TS, Korban SS (2004) Enhancing the frequency of somatic embryogenesis following Agrobacterium-mediated transformation of immature cotyledons of soybean [Glycine max (L.) Merrill]. In Vitro Cell Dev Biol-Plant 40:552–558CrossRefGoogle Scholar
  50. Ko TS, Lee S, Krasnyanski S, Korban SS (2003) Two critical factors are required for efficient transformation of multiple soybean cultivars: Agrobacterium strain and orientation of immature cotyledonary explant. Theor Appl Genet 107:439–447PubMedCrossRefGoogle Scholar
  51. Komatsuda T, Ko SW (1990) Screening of soybean (Glycine max (L.) Merrill) genotypes for embryo production form immature embryo. Jpn J Breed 40:249–251CrossRefGoogle Scholar
  52. Kumar B, Talukdar A, Verma K, Girmilla V, Bala I, Lal SK, Pal Singh K, Sapra RL (2014) Screening of soybean [Glycine max (L.) Merr.] genotypes for yellow mosaic virus (YMV) disease resistance and their molecular characterization using RGA and SSRs markers. Aust J Crop Sci 8:27–34Google Scholar
  53. Kumar V, Sharma A, Prasad BCN, Gururaj HB, Ravishankar GA (2006) Agrobacterium rhizogenes-mediated genetic transformation resulting in hairy root formation is enhanced by ultrasonication and acetosyringone treatment. Electron J Biotechnol 9:349–357CrossRefGoogle Scholar
  54. Kumari S, Krishnan V, Dahuja A, Vinutha T, Jolly M, Sachdev A (2016) A rapid method for optimization of Agrobacterium-mediated transformation of Indian soybean genotypes. Indian J Biochem Biophys 53:218–226Google Scholar
  55. Kumria R, Waie B, Rajam MV (2001) Plant regeneration from transformed embryogenic callus of an elite Indica rice via Agrobacterium. Plant Cell Tissue Organ Cult 67:63–71CrossRefGoogle Scholar
  56. Kuta DD, Tripathi L (2005) Agrobacterium-induced hypersensitive necrotic reaction in plant cells: a resistance response against Agrobacterium-mediated DNA transfer. Afr J Biotechnol 4:752–757Google Scholar
  57. Lee SH, Lee DG, Woo HS, Lee KW, Kim DH, Kwak SS, Kim JS, Kim H, Ahsan N, Choi MS, Yang JK (2006) Production of transgenic orchard grass via Agrobacterium-mediated transformation of seed-derived callus tissues. Plant Sci 171:408–414PubMedCrossRefGoogle Scholar
  58. Lee YW, Jin S, SimWS NEW (1995) Genetic evidence for direct sensing of phenolic compounds by the VirA protein of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 92:12245–12249PubMedPubMedCentralCrossRefGoogle Scholar
  59. Leelavathi S, Sunnichan SG, Kumria R, Vijaykanth GP, Bhatnagar RK, Reddy VS (2004) A simple and rapid Agrobacterium-mediated transformation protocol for cotton (Gossypium hirsutum L.): Embryogenic calli as a source to generate large numbers of transgenic plants. Plant Cell Rep 22:465–470PubMedCrossRefGoogle Scholar
  60. Li S, Cong Y, Liu Y, Wang T, Shuai Q, Chen N, Gai J, Li Y (2017) Optimization of Agrobacterium-mediated transformation in soybean. Front Plant Sci 8:246PubMedPubMedCentralGoogle Scholar
  61. Liu HK, Yang C, Wei ZM (2004) Efficient Agrobacterium tumefaciens-mediated transformation of soybeans using an embryonic tip regeneration system. Planta 219:1042–1049PubMedCrossRefPubMedCentralGoogle Scholar
  62. Liu Z, Park BJ, Kanno A, Kameya T (2005) The novel use of a combination of sonication and vacuum infiltration in Agrobacterium-mediated transformation of kidney bean (Phaseolus vulgaris L.) with lea gene. Mol Breeding 16:189–197CrossRefGoogle Scholar
  63. Mariashibu TS, Subramanyam K, Arun M, Mayavan S, Rajesh M, Theboral J, Manickavasagam M, Ganapathi A (2013) Vacuum infiltration enhances the Agrobacterium-mediated genetic transformation in Indian soybean cultivars. Acta Physiol Plant 35:41–54CrossRefGoogle Scholar
  64. Mayavan S, Subramanyam K, Arun M, Rajesh M, Dev GK, Sivanandhan G, Jaganath B, Manickavasagam M, Selvaraj N, Ganapathi A (2013) Agrobacterium tumefaciens-mediated in planta seed transformation strategy in sugarcane. Plant Cell Rep 32:1557–1574PubMedCrossRefGoogle Scholar
  65. Mayer AM, Harel E (1979) Polyphenol oxidases in plants. Phytochemistry 18:193–215CrossRefGoogle Scholar
  66. Mccabe DE, Swain WF, Martinell BJ, Christou P (1988) Stable transformation of soybean (Glycine max) by particle acceleration. Nat Biotechnol 6:923–926CrossRefGoogle Scholar
  67. Meurer CA, Dinkins RD, Collin GB (1998) Factors affecting soybean cotyledonary node transformation. Plant Cell Rep 18:180–186CrossRefGoogle Scholar
  68. Mohiuddin KM, Abdullah C, Harikrishna K, Chowdhury K, Napis S (2011) Enhanced virulence gene activity of Agrobacterium in muskmelon (Cucumis melo L.) cv. ‘Birdie’. Not Sci Biol 3:71–79CrossRefGoogle Scholar
  69. Mukeshimana G, Ma Y, Walworth AE, Song GQ, Kelly JD (2013) Factors influencing regeneration and Agrobacterium tumefaciens-mediated transformation of common bean Phaseolus vulgaris L. Plant Biotechnol Rep 7:59–70CrossRefGoogle Scholar
  70. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  71. Negishi O, Ozawa T (2000) Inhibition of enzymatic browning and protection of sulfhydryl enzymes by thiol compounds. Phytochemistry 54:481–487PubMedCrossRefPubMedCentralGoogle Scholar
  72. Olhoft PM, Flagel LE, Donovan CM, Somers DA (2003) Efficient soybean transformation using hygromycin B selection in the cotyledonary node method. Planta 216:723–735PubMedPubMedCentralGoogle Scholar
  73. Olhoft PM, Somers DA (2001) L-cysteine increases Agrobacterium-mediated T-DNA delivery into soybean cotyledonary node cells. Plant Cell Rep 20:706–711CrossRefGoogle Scholar
  74. Öz MT, Eyidoğan F, Yücel M, Öktem HA (2009) Optimized selection and regeneration conditions for Agrobacterium-mediated transformation of chickpea cotyledonary nodes. Pak J Bot 41:2043–2054Google Scholar
  75. Park BJ, Liu Z, Kanno A, Kameya T (2005) Transformation of radish (Raphanus sativus L.) via sonication and vacuum infiltration of germinated seeds with Agrobacterium harboring a group 3 LEA gene from B. napus. Plant Cell Rep 24:494–500PubMedCrossRefPubMedCentralGoogle Scholar
  76. Paz MM, Martinez JC, Kalvig AB, Fonger TM, Wang K (2006) Improved cotyledonary node method using an alternative explant derived from mature seed for efficient Agrobacterium-mediated soybean transformation. Plant Cell Rep 25:206–213PubMedCrossRefPubMedCentralGoogle Scholar
  77. Potrykus I (1990) Gene transfer to cereals: an assessment. Nat Biotechnol 8:535–542CrossRefGoogle Scholar
  78. Raj SK, Singh R, Pandey SK, Singh BP (2005) Agrobacterium-mediated tomato transformation and regeneration of transgenic lines expressing tomato leaf curl virus coat protein gene for resistance against TLCV infection. Curr Sci India 88:1674–1679Google Scholar
  79. Rashid H, Yoki S, Toriyama K, Hinata K (1996) Transgenic plant production mediated by Agrobacterium in Indica rice. Plant Cell Rep 15:727–730PubMedCrossRefPubMedCentralGoogle Scholar
  80. Richard-Forget FC, Goupy PM, Nicolas JJ (1992) Cysteine as an inhibitor of enzymatic browning. 2. Kinetic studies. J Agr Food Chem 40:2108–2113CrossRefGoogle Scholar
  81. Sahoo KK, Tripathi AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) An improved protocol for efficient transformation and regeneration of diverse indica rice cultivars. Plant Methods 7:49–59PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  83. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  84. Santarem ER, Trick HN, Essig JS, Finer JJ (1998) Sonication-assisted Agrobacterium-mediated transformation of soybean immature cotyledons: optimization of transient expression. Plant Cell Rep 17:752–759CrossRefGoogle Scholar
  85. Sato S, Newell C, Kolacz K, Tredo L, Finer J, Hinchee M (1993) Stable transformation via particle bombardment in two different soybean regeneration systems. Plant Cell Rep 12:408–413PubMedPubMedCentralGoogle Scholar
  86. Sheng J, Citovsky V (1996) Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8:1699–1710PubMedPubMedCentralCrossRefGoogle Scholar
  87. Shrawat AK, Becke D, Lorz H (2007) Agrobacterium tumefaciens-mediated genetic transformation of barley (Hordeum vulgare L.). Plant Sci 172:281–290CrossRefGoogle Scholar
  88. Solís JIF, Mlejnek P, Studená K, Procházka S (2003) Application of sonication-assisted Agrobacterium-mediated transformation in Chenopodium rubrum L. Plant Soil Environ 49:255–260CrossRefGoogle Scholar
  89. Stachel SE, Messens E, Van MM, Zambryski P (1985) Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature 318:624–629CrossRefGoogle Scholar
  90. Subramanyam K, Sailaja KV, Srinivasulu M, Lakshmidevi K (2011) Highly efficient Agrobacterium-mediated transformation of banana cv. Rasthali (AAB) via sonication and vacuum infiltration. Plant Cell Rep 30:425–436PubMedCrossRefPubMedCentralGoogle Scholar
  91. Tague BW, Mantis J (2006) In Planta Agrobacterium-mediated transformation by vacuum infiltration. Methods Mol Biol 323:215–223PubMedPubMedCentralGoogle Scholar
  92. Tiwari V, Chaturvedi AK, Mishra A, Jha B (2015) An efficient method of Agrobacterium-mediated genetic transformation and regeneration in local Indian cultivar of groundnut (Arachis hypogaea) using grafting. Appl Biochem Biotechnol 175:436–453PubMedCrossRefPubMedCentralGoogle Scholar
  93. Townsend JA, Thomas LA (1993) An improved method of Agrobacterium-mediated transformation of cultured soybean cells. US Patent WO 94:02620Google Scholar
  94. Trick HN, Finer JJ (1997) SAAT: sonication-assisted Agrobacterium-mediated transformation. Transgenic Res 6:329–336CrossRefGoogle Scholar
  95. Tyagi H, Rajsubramaniam S, Dasgupta I (2007) Regeneration and Agrobacterium-mediated transformation of a popular indica rice variety, ADT39. Curr Sci India 93:678–673Google Scholar
  96. Wang G, Huang M (2002) Tissue culture and plant regeneration of Cerasus campanulata. J Nanjing Univ 26:73–76Google Scholar
  97. Wang Q, Xing S, Pan Q, Yuan F, Zhao J, Tian Y, Chen Y, Wang G, Tang K (2012) Development of efficient Catharanthus roseus regeneration and transformation system using Agrobacterium tumefaciens and hypocotyls as explants. BMC Biotechnol 12:34PubMedPubMedCentralCrossRefGoogle Scholar
  98. Weir B, Wang X, Upadhyaya N, Elliot A, Brettell R (2001) Agrobacterium tumefaciens transformation of wheat using suspension cells as a model system and green fluorescent protein as a visual marker. Aust J Plant Physiol 28:807–818Google Scholar
  99. Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–691PubMedPubMedCentralCrossRefGoogle Scholar
  100. Wroblewski T, Tomczak A, Michelmore R (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotech J 3:259–273CrossRefGoogle Scholar
  101. Xinping YI, Deyue YU (2006) Transformation of multiple soybean cultivars by infecting cotyledonary-node with Agrobacterium tumefaciens. Afr J Biotechnol 5:1989–1993Google Scholar
  102. Xue RG, Xie HF, Zhang B (2006) A multi-needle assisted transformation of soybean cotyledonary node cells. Biotechnol Lett 28:1551–1557PubMedCrossRefPubMedCentralGoogle Scholar
  103. Yan B, Reddy MSS, Collins GB, Dinkins RD (2000) Agrobacterium tumefaciens-mediated transformation of soybean [Glycine max (L.) Merrill.] using immature zygotic cotyledon explants. Plant Cell Rep 19:1090–1097CrossRefGoogle Scholar
  104. Ye X, Williams EJ, Shen J, Esser JA, Nichols AM, Petersen MW, Gilbertson LA (2008) Plant development inhibitory genes in binary vector backbone improve quality event efficiency in soybean transformation. Transgenic Res 17:827–838PubMedCrossRefPubMedCentralGoogle Scholar
  105. Zhang Z, Xing A, Staswick P, Clemente TE (1999) The use of glufosinate as a selective agent in Agrobacterium-mediated transformation of soybean. Plant Cell Tissue Organ Cult 56:37–46CrossRefGoogle Scholar
  106. Zhong H, Que Q (2009) Method for transforming soybean (Glycine max). US Patent Number 20090023212Google Scholar
  107. Zia M, Zarrin RF, Rehman RU, Chaudhary FM (2010) Agrobacterium-mediated transformation of soybean (Glycine max L.): some conditions standardization. Pak J Bot 42:2269–2279Google Scholar

Copyright information

© The Society for In Vitro Biology 2018

Authors and Affiliations

  • Alkesh Hada
    • 1
    • 2
  • Veda Krishnan
    • 1
  • M. S. Mohamed Jaabir
    • 2
  • Archana Kumari
    • 3
  • Monica Jolly
    • 1
  • Shelly Praveen
    • 1
  • Archana Sachdev
    • 1
  1. 1.Division of BiochemistryIndian Agricultural Research InstituteNew DelhiIndia
  2. 2.Department of BiotechnologyNational College (Autonomous)TiruchirappalliIndia
  3. 3.Division of PathologyIndian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations