Tissue culture-based Agrobacterium-mediated and in planta transformation methods

https://doi.org/10.17221/177/2016-CJGPBCitation:Niazian M., Sadat Noori S.A., Galuszka P., Mortazavian S.M.M. (2017): Tissue culture-based Agrobacterium-mediated and in planta transformation methods. Czech J. Genet. Plant Breed., 53: 133-143.
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Gene transformation can be done in direct and indirect (Agrobacterium-mediated) ways. The most efficient method of gene transformation to date is Agrobacterium-mediated method. The main problem of Agrobacterium-method is that some plant species and mutant lines are recalcitrant to regeneration. Requirements for sterile conditions for plant regeneration are another problem of Agrobacterium-mediated transformation. Development of genotype-independent gene transformation method is of great interest in many plants. Some tissue culture-independent Agrobacterium-mediated gene transformation methods are reported in individual plants and crops. Generally, these methods are called in planta gene transformation. In planta transformation methods are free from somaclonal variation and easier, quicker, and simpler than tissue culture-based transformation methods. Vacuum infiltration, injection of Agrobacterium culture to plant tissues, pollen-tube pathway, floral dip and floral spray are the main methods of in planta transformation. Each of these methods has its own advantages and disadvantages. Simplicity and reliability are the primary reasons for the popularity of the in planta methods. These methods are much quicker than regular tissue culture-based Agrobacterium-mediated gene transformation and success can be achieved by non-experts. In the present review, we highlight all methods of in planta transformation comparing them with regular tissue culture-based Agrobacterium-mediated transformation methods and then recently successful transformations using these methods are presented.
Ali Asjad, Bang Sun Woong, Chung Sang-Min, Staub Jack E. (2015): Plant Transformation via Pollen Tube-Mediated Gene Transfer. Plant Molecular Biology Reporter, 33, 742-747  https://doi.org/10.1007/s11105-014-0839-5
Arun Muthukrishnan, Subramanyam Kondeti, Mariashibu Thankaraj Salammal, Theboral Jeevaraj, Shivanandhan Ganeshan, Manickavasagam Markandan, Ganapathi Andy (2015): Application of Sonication in Combination with Vacuum Infiltration Enhances the Agrobacterium-Mediated Genetic Transformation in Indian Soybean Cultivars. Applied Biochemistry and Biotechnology, 175, 2266-2287  https://doi.org/10.1007/s12010-014-1360-x
Baranski R. (2008): Genetic transformation of carrot (Daucus carota) and other Apiaceae species. Transgenic Plant Journal, 2: 18–38.
Baskaran P., Soós V., Balázs E., Van Staden J. (2016): Shoot apical meristem injection: A novel and efficient method to obtain transformed cucumber plants. South African Journal of Botany, 103, 210-215  https://doi.org/10.1016/j.sajb.2015.09.006
Bechtold N., Pelletier G. (1998): In-planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods in Molecular Biology, 82: 259–326.
Bechtold N., Ellis J., Pelletier G. (1993): In-planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Comptes rendus de l’Académie des sciences. Série 3, Sciences de la vie, 316: 1194–1199.
Bibi N., Kai F., Shuna Y., Mi N., Mosaddek I.M.,Waqas M., Xuede W. (2013): An efficient and highly reproducible approach for the selection of upland transgenic cotton produced by pollen tube pathway method. Australian Journal of Crop Science, 7: 1714–1722.
Bidney Dennis, Scelonge Chris, Martich Joanie, Burrus Monique, Sims Lynn, Huffman Gary (1992): Microprojectile bombardment of plant tissues increases transformation frequency by Agrobacterium tumefaciens. Plant Molecular Biology, 18, 301-313  https://doi.org/10.1007/BF00034957
Chee P. P., Fober K. A., Slightom J. L. (1989): Transformation of Soybean (Glycine max) by Infecting Germinating Seeds with Agrobacterium tumefaciens. PLANT PHYSIOLOGY, 91, 1212-1218  https://doi.org/10.1104/pp.91.3.1212
Chung M.H., Chen M.K., Pan S.E. (2000): Floral spray transformation can efficiently generate Arabidopsis transgenic plants. Transgenic Research, 9: 471–476. https://doi.org/10.1023/A:1026522104478
Clement Wong Kiing Fook, Lai Kok Song, Wong Mui Yun, Maziah Mahmood (2016): Heat and hydrolytic enzymes treatment improved the Agrobacterium-mediated transformation of recalcitrant indica rice (Oryza sativa L.). Plant Cell, Tissue and Organ Culture (PCTOC), 125, 183-190  https://doi.org/10.1007/s11240-015-0926-9
Clough Steven J., Bent Andrew F. (1998): Floral dip: a simplified method forAgrobacterium-mediated transformation ofArabidopsis thaliana. The Plant Journal, 16, 735-743  https://doi.org/10.1046/j.1365-313x.1998.00343.x
Gelvin Stanton B. (2000): A GROBACTERIUMAND P LANT G ENES I NVOLVED IN T-DNA T RANSFER AND I NTEGRATION. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 223-256  https://doi.org/10.1146/annurev.arplant.51.1.223
Gould Jean, Banister Sharon, Hasegawa Osamu, Fahima Michal, Smith RobertaH. (1991): Regeneration of Gossypium hirsutum and G. barbadense from shoot apex tissues for transformation. Plant Cell Reports, 10, -  https://doi.org/10.1007/BF00233024
GUO Bing-fu, GUO Yong, WANG Jun, ZHANG Li-juan, JIN Long-guo, HONG Hui-long, CHANG Ru-zheng, QIU Li-juan (2015): Co-treatment with surfactant and sonication significantly improves Agrobacterium-mediated resistant bud formation and transient expression efficiency in soybean. Journal of Integrative Agriculture, 14, 1242-1250  https://doi.org/10.1016/S2095-3119(14)60907-2
Hadi Masood Z., McMullen Michael D., Finer John J. (1996): Transformation of 12 different plasmids into soybean via particle bombardment. Plant Cell Reports, 15, 500-505  https://doi.org/10.1007/BF00232982
Hooykaas P J J, Beijersbergen A G M (1994): The Virulence System of Agrobacterium Tumefaciens. Annual Review of Phytopathology, 32, 157-181  https://doi.org/10.1146/annurev.py.32.090194.001105
(1985): A Simple and General Method for Transferring Genes into Plants. Science, 227, 1229-1231  https://doi.org/10.1126/science.227.4691.1229
Shah Sabir Hussain, Ali Shaukat, Jan Sohail Ahmad, Jalal-Ud-Din , Ali Ghulam Muhammad (2015): Piercing and incubation method of in planta transformation producing stable transgenic plants by overexpressing DREB1A gene in tomato (Solanum lycopersicum Mill.). Plant Cell, Tissue and Organ Culture (PCTOC), 120, 1139-1157  https://doi.org/10.1007/s11240-014-0670-6
Joersbo Morten, Brunstedt Janne (1990): Direct gene transfer to plant protoplasts by mild sonication. Plant Cell Reports, 9, -  https://doi.org/10.1007/BF00232181
Joersbo Morten, Brunstedt Janne (1992): Sonication: A new method for gene transfer to plants. Physiologia Plantarum, 85, 230-234  https://doi.org/10.1111/j.1399-3054.1992.tb04727.x
Jouzani Gholamreza Salehi (2013): Plant Molecular Farming: Future Prospects and Biosafety Challenges. Biosafety, 02, -  https://doi.org/10.4172/2167-0331.1000e136
Kalbande Bipinchandra B., Patil Anita S. (2016): Plant tissue culture independent Agrobacterium tumefaciens mediated In-planta transformation strategy for upland cotton (Gossypium hirsutum). Journal of Genetic Engineering and Biotechnology, 14, 9-18  https://doi.org/10.1016/j.jgeb.2016.05.003
Kapildev Gnanajothi, Chinnathambi Arunachalam, Sivanandhan Ganeshan, Rajesh Manoharan, Vasudevan Venkatachalam, Mayavan Subramanian, Arun Muthukrishnan, Jeyaraj Murugaraj, Alharbi Sulaiman Ali, Selvaraj Natesan, Ganapathi Andy (2016): High-efficient Agrobacterium-mediated in planta transformation in black gram (Vigna mungo (L.) Hepper). Acta Physiologiae Plantarum, 38, -  https://doi.org/10.1007/s11738-016-2215-6
Kim Mee-Jin, An Dong-Ju, Moon Ki-Beom, Cho Hye-Sun, Min Sung-Ran, Sohn Jung-Hoon, Jeon Jae-Heung, Kim Hyun-Soon (2016): Highly efficient plant regeneration and Agrobacterium-mediated transformation of Helianthus tuberosus L.. Industrial Crops and Products, 83, 670-679  https://doi.org/10.1016/j.indcrop.2015.12.054
Kojima M., Sparthana P., Teixeira da Silva JA., Nogawa M. (2006): Development of in planta transformation methods using Agrobacterium tumefaciens. In: Teixeira da Silva J.A. (ed.): Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues. Isleworth, Global Science Books: 41–48.
Kumar Vinay, Jain Mukesh (2015): The CRISPR–Cas system for plant genome editing: advances and opportunities. Journal of Experimental Botany, 66, 47-57  https://doi.org/10.1093/jxb/eru429
Lin Jianzhong, Zhou Bo, Yang Yuanzhu, Mei Jin, Zhao Xiaoying, Guo Xinhong, Huang Xingqun, Tang Dongying, Liu Xuanming (2009): Piercing and vacuum infiltration of the mature embryo: a simplified method for Agrobacterium-mediated transformation of indica rice. Plant Cell Reports, 28, 1065-1074  https://doi.org/10.1007/s00299-009-0706-2
Liu J., Su Q., An L., Yang A. (2009a): Transfer of a minimal linear marker-free and vector-free smGFP cassette into soybean via ovary-drip transformation. Biotechnology Letters, 31: 295–303.
Liu M., Yang J., Cheng Y.Q., An L.J. (2009b): Optimization of soybean (Glycine max (L.) Merrill) in planta ovary transformation using a linear minimal gus gene cassette. Journal of Zhejiang University Science B, 10: 870–876.
Liu X., Brost J., Hutcheon C., Guilfoil R., Wilson A.K., Leung S., Shewmaker C.K., Rooke S., Nguyen T., Kiser J., Rocher J.D. (2012): Transformation of the oilseed crop Camelina sativa by Agrobacterium-mediated floral dip and simple large-scale screening of transformants. In Vitro Cellular & Developmental Biology − Plant, 48: 462–468.
Lowe Keith, Wu Emily, Wang Ning, Hoerster George, Hastings Craig, Cho Myeong-Je, Scelonge Chris, Lenderts Brian, Chamberlin Mark, Cushatt Josh, Wang Lijuan, Ryan Larisa, Khan Tanveer, Chow-Yiu Julia, Hua Wei, Yu Maryanne, Banh Jenny, Bao Zhongmeng, Brink Kent, Igo Elizabeth, Rudrappa Bhojaraja, Shamseer PM, Bruce Wes, Newman Lisa, Shen Bo, Zheng Peizhong, Bidney Dennis, Falco Carl, Register Jim, Zhao Zuo-Yu, Xu Deping, Jones Todd, Gordon-Kamm William (2016): Morphogenic Regulators Baby boom and Wuschel Improve Monocot Transformation. The Plant Cell, 28, 1998-2015  https://doi.org/10.1105/tpc.16.00124
Luo Zhong-xun, Wu Ray (1988): A simple method for the transformation of rice via the pollen-tube pathway. Plant Molecular Biology Reporter, 6, 165-174  https://doi.org/10.1007/BF02669590
Manickavasagam Markandan, Subramanyam Kondeti, Ishwarya Rajagobalan, Elayaraja Dhandapani, Ganapathi Andy (2015): Assessment of factors influencing the tissue culture-independent Agrobacterium-mediated in planta genetic transformation of okra [Abelmoschus esculentus (L.) Moench]. Plant Cell, Tissue and Organ Culture (PCTOC), 123, 309-320  https://doi.org/10.1007/s11240-015-0836-x
Mariashibu Thankaraj Salammal, Subramanyam Kondeti, Arun Muthukrishnan, Mayavan Subramanian, Rajesh Manoharan, Theboral Jeevaraj, Manickavasagam Markandan, Ganapathi Andy (2013): Vacuum infiltration enhances the Agrobacterium-mediated genetic transformation in Indian soybean cultivars. Acta Physiologiae Plantarum, 35, 41-54  https://doi.org/10.1007/s11738-012-1046-3
Mayavan Subramanian, Subramanyam Kondeti, Arun Muthukrishnan, Rajesh Manoharan, Kapil Dev Gnanajothi, Sivanandhan Ganeshan, Jaganath Balusamy, Manickavasagam Markandan, Selvaraj Natesan, Ganapathi Andy (2013): Agrobacterium tumefaciens-mediated in planta seed transformation strategy in sugarcane. Plant Cell Reports, 32, 1557-1574  https://doi.org/10.1007/s00299-013-1467-5
Mayavan Subramanian, Subramanyam Kondeti, Jaganath Balusamy, Sathish Dorairaj, Manickavasagam Markandan, Ganapathi Andy (2015): Agrobacterium-mediated in planta genetic transformation of sugarcane setts. Plant Cell Reports, 34, 1835-1848  https://doi.org/10.1007/s00299-015-1831-8
Meyers Benjamin, Zaltsman Adi, Lacroix Benoît, Kozlovsky Stanislav V., Krichevsky Alexander (2010): Nuclear and plastid genetic engineering of plants: Comparison of opportunities and challenges. Biotechnology Advances, 28, 747-756  https://doi.org/10.1016/j.biotechadv.2010.05.022
Mohanty D., Chandra A., Tandon R. (2016): Germline transformation for crop improvement. In: Rajpal R.V., Rao R.S., Raina S.N. (eds): Molecular Breeding for Sustainable Crop Improvement. Cham, Springer International Publishing: 343–395.
Mrízová Katarína, Holasková Edita, Öz M. Tufan, Jiskrová Eva, Frébort Ivo, Galuszka Petr (2014): Transgenic barley: A prospective tool for biotechnology and agriculture. Biotechnology Advances, 32, 137-157  https://doi.org/10.1016/j.biotechadv.2013.09.011
Mu Guiqin, Chang Naidi, Xiang Kui, Sheng Yaou, Zhang Zhiming, Pan Guangtang (2012): Genetic Transformation of Maize Female Inflorescence Following Floral Dip Method Mediated by Agrobacterium. Biotechnology(Faisalabad), 11, 178-183  https://doi.org/10.3923/biotech.2012.178.183
Naing Aung Htay, Ai Trinh Ngoc, Jeon Su Min, Lim Sun Hyung, Kim Chang Kil (2016): An efficient protocol for Agrobacterium-mediated genetic transformation of recalcitrant chrysanthemum cultivar Shinma. Acta Physiologiae Plantarum, 38, -  https://doi.org/10.1007/s11738-015-2059-5
Nanasato Yoshihiko, Konagaya Ken-ichi, Okuzaki Ayako, Tsuda Mai, Tabei Yutaka (2013): Improvement of Agrobacterium-mediated transformation of cucumber (Cucumis sativus L.) by combination of vacuum infiltration and co-cultivation on filter paper wicks. Plant Biotechnology Reports, 7, 267-276  https://doi.org/10.1007/s11816-012-0260-1
Niapour N., Baghizadeh A., Tohidfar M., Pourseyedi Sh. (2013): Agrobacterium mediated transformation of fld and gus genes into canola for salinity stress. Journal of Stress Physiology & Biochemistry, 9: 74–85.
Palla Kaitlin J., Pijut Paula M. (2015): Agrobacterium-mediated genetic transformation of Fraxinus americana hypocotyls. Plant Cell, Tissue and Organ Culture (PCTOC), 120, 631-641  https://doi.org/10.1007/s11240-014-0630-1
Rao Abdul Qayyum, Bakhsh Allah, Kiani Sarfraz, Shahzad Kamran, Shahid Ahmad Ali, Husnain Tayyab, Riazuddin S. (2009): The myth of plant transformation. Biotechnology Advances, 27, 753-763  https://doi.org/10.1016/j.biotechadv.2009.04.028
Ravanfar Seyed Ali, Aziz Maheran Abdul (2015): Shoot tip regeneration and optimization of Agrobacterium tumefaciens-mediated transformation of Broccoli (Brassica oleracea var. italica) cv. Green Marvel. Plant Biotechnology Reports, 9, 27-36  https://doi.org/10.1007/s11816-014-0340-5
Richardson K., Fowler S., Pullen C., Skelton C., Morris B., Putterill J. (1998): T-DNA tag-ging of a flowering-time gene and improved gene transfer by in planta transformation of Arabidopsis. Functional Plant Biology, 25: 125–130.
Sainger Manish, Chaudhary Darshna, Dahiya Savita, Jaiwal Ranjana, Jaiwal Pawan K. (2015): Development of an efficient in vitro plant regeneration system amenable to Agrobacterium- mediated transformation of a recalcitrant grain legume blackgram (Vigna mungo L. Hepper). Physiology and Molecular Biology of Plants, 21, 505-517  https://doi.org/10.1007/s12298-015-0315-1
Sivanandhan Ganeshan, Kapil Dev Gnajothi, Theboral Jeevaraj, Selvaraj Natesan, Ganapathi Andy, Manickavasagam Markandan, Munderloh Ulrike Gertrud (2015): Sonication, Vacuum Infiltration and Thiol Compounds Enhance the Agrobacterium-Mediated Transformation Frequency of Withania somnifera (L.) Dunal. PLOS ONE, 10, e0124693-  https://doi.org/10.1371/journal.pone.0124693
Sobhanian N., Habashy A.A., Farshad Far E., Tohidfar M. (2012): Optimizing regeneration and reporter gene (gus) transformation of alfalfa (Medicago sativa). Annals of Biological Research, 3: 2419–2427.
Stachel Scott E., Messens Eric, Van Montagu Marc, Zambryski Patricia (1985): Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature, 318, 624-629  https://doi.org/10.1038/318624a0
Tague B., Mantis J. (2006): In planta Agrobacterium-mediated transformation by vacuum infiltration. In: Salinas J., Sanchez-Serrano J.J. (eds): Arabidopsis Protocols. New York, Humana Press: 215–223.
Tohidfar M., Mohsenpour M. (2010): Effective factors in cotton (Gossipium spp.) transformation using Agrobacterium. Journal of Agricultural Biotechnology, 2: 1–24. (in Farsi, Abstract in English)
Tohidfar M., Khosravi S. (2015): Transgenic crops with an improved resistance to biotic stresses. A review. Biotechnologie, Agronomie, Société et Environnement, 19: 62–70.
Tohidfar M., Ghareyazie B., Mosavi M., Yazdani Sh., Golabchian R. (2008): Agrobacterium-mediated transformation of cotton (Gossypium hirsutum) using a synthetic cry1Ab gene for enhanced resistance against Heliothis armigera. Iranian Journal of Biotechnology, 6: 164–173.
Trick H.N., Finer J.J. (1997): SAAT: sonication-assisted Agrobacterium-mediated transformation. Transgenic Research, 6: 329–336. https://doi.org/10.1023/A:1018470930944
Tripathi Leena, Singh Aditya K., Singh Shweta, Singh Rani, Chaudhary Sonam, Sanyal Indraneel, Amla D. V. (2013): Optimization of regeneration and Agrobacterium-mediated transformation of immature cotyledons of chickpea (Cicer arietinum L.). Plant Cell, Tissue and Organ Culture (PCTOC), 113, 513-527  https://doi.org/10.1007/s11240-013-0293-3
Martinez-Trujillo Miguel, Limones-Briones Veronica, Cabrera-Ponce José Luis, Herrera-Estrella Luis (2004): Improving transformation efficiency ofArabidopsis thaliana by modifying the floral dip method. Plant Molecular Biology Reporter, 22, 63-70  https://doi.org/10.1007/BF02773350
Tzfira Tzvi, Citovsky Vitaly (2002): Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends in Cell Biology, 12, 121-129  https://doi.org/10.1016/S0962-8924(01)02229-2
Wang M., Zhang B., Wang Q. (2013): Cotton transformation via pollen tube pathway. In: Zhang B (ed.): Transgenic Cotton: Methods and Protocols, Methods in Molecular Biology. New York, Humana Press: 71–77.
Xu K., Huang X., Wu M., Wang Y., Chang Y., Liu K., Zhang J., Zhang Y., Zhang F., Yi L., Li T., Wang R., Tan G., Li C. (2014): A rapid, highly efficient and economical method of Agrobacterium-mediated in planta transient transformation in living onion epidermis. PLoS ONE, 9: e83556.
Zalabák David, Pospíšilová Hana, Šmehilová Mária, Mrízová Katarína, Frébort Ivo, Galuszka Petr (2013): Genetic engineering of cytokinin metabolism: Prospective way to improve agricultural traits of crop plants. Biotechnology Advances, 31, 97-117  https://doi.org/10.1016/j.biotechadv.2011.12.003
Zale Janice M., Agarwal S., Loar S., Steber C. M. (2009): Evidence for stable transformation of wheat by floral dip in Agrobacterium tumefaciens. Plant Cell Reports, 28, 903-913  https://doi.org/10.1007/s00299-009-0696-0
Zhang Li-Jian, Cheng Le-Mei, Xu Ning, Zhao Nan-Ming, Li Chang-Gong, Yuan Jing, Jia Shi-Rong (1991): Efficient Transformation of Tobacco by Ultrasonication. Bio/Technology, 9, 996-997  https://doi.org/10.1038/nbt1091-996
Zhou G.Y., Weng J., Zeng Y., Huang J., Qian S., Liu G. (1983): Introduction of exogenous DNA into cotton embryos. Methods in Enzymology, 101: 433–481.
Zupan John, Muth Theodore R., Draper Olga, Zambryski Patricia (2000): The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. The Plant Journal, 23, 11-28  https://doi.org/10.1046/j.1365-313x.2000.00808.x
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