Review Article: Genetic Engineering in Cereals: Focusing on Agrobacterium Application

Document Type : Review

Authors

1 Iiranian Company for Maize Development, Seed Laboratory, Kermanshah, Iran.

2 Department of Plant Production and Genetics, Campus of Agriculture and Natural Resources, Razi University, Kermanshah, Iran.

3 Horticulture and Crop Research Department, Kermanshah Agricultural and Natural Resources Research and Education Center (AREEO), Kermanshah, Iran.

10.22126/cbb.2025.11721.1102

Abstract

Improving the quality and performance of plant products has significant and beneficial implications for food security and sustainable agriculture. Accordingly, plant genetic modification is a key issue in agricultural research to achieve these goals. To date, conventional breeding methods and genetic engineering have developed plants with higher yield and performance, better seed quality, and higher resistance to pests and diseases. The process of gene transfer in genetic engineering refers to a series of genetic procedures through which a specific segment of DNA, carrying a new gene or a novel structure of genes, is artificially inserted into the genome of a living organism using laboratory techniques. In this genetic process, the recipient of the new gene is referred to as a transgenic organism. Two systems are employed in this process: direct and indirect gene transfer methods. Gene transfer via Agrobacterium is one of the successful methods for transferring genes in plants. This bacterium is regarded as nature's smallest genetic engineer. In the gene transfer technique to plants using Agrobacterium, the natural system of this bacterium is utilised to facilitate the transfer of the target gene. The application of this method by plant breeding researchers has led to beneficial genetic changes in various plant species. This technique offers numerous advantages over other gene transfer methods, including the stability of transgenic plants, simplicity, and cost-effectiveness. However, there are limitations to this technology, such as lower efficiency of transgene, limited effectiveness in monocotyledonous plants, and dependence on genotype and explant. To address these limitations, genetic engineers are striving to overcome the complex mechanisms and challenges associated with this method, aiming to provide effective solutions for the targeted insertion of DNA into appropriate plant genomic locations. Given the importance of gene transfer via Agrobacterium and the need to enhance the efficiency of this method, investigating the mechanisms of gene transfer with this bacterium is essential. A deeper understanding of Agrobacterium biology can facilitate the expansion of gene transfer applications through this system. Furthermore, advancements in this gene transfer method require manipulation and iterative testing throughout the biological process. Therefore, the upcoming review article offers comprehensive information on gene transfer methods, the process of plant transgenics via Agrobacterium, the types of plants that have been modified using this technique, as well as the associated challenges and issues. This article will be beneficial for individuals working on plant genome editing using Agrobacterium and the CRISPR/Cas9 technique.

Keywords

Main Subjects


Aalami, O., Azadi, P., Hadizadeh, H., Wilde, H.D., Karimian, Z., Nemati, H., & Samiei, L.2023. Melatonin strongly enhances the Agrobacterium-mediated transformation of carnation in nitrogen-depleted media. BMC Plant Biology, 23(1), p.316. https://doi.org/10.1186/s12870-023-04325-5
Akbarzadeh, A., Rezaei-Sadabady, R., Davaran, S., Joo, S.W., Zarghami, N., Hanifehpour, Y., Samiei, M., Kouhi, M., & Nejati-Koshki, K. 2016. Liposome: Classification, preparation, & alications. Nanoscale Research Letter, 8, 102. http://www.nanoscalereslett.com/content/8/1/102
Ali, A., Bang, S.W., Chung, S. M & Staub, J.E. 2015. Plant Transformation via Pollen Tube-Mediated Gene Transfer. Plant Molecular & Biology Reports, 33, 742–747. https://doi.org/10.1080/01904167.2022.2096467
Allam, M.A., & Saker, M.M. 2017. Microprojectile Bombardment Transformation of Date Palm Using the Insecticidal Cholesterol Oxidase (ChoA) Gene. In: Al-Khayri, J., Jain, S., Johnson, D. (eds) Date Palm Biotechnology Protocols Volume I. Methods in Molecular Biology, vol 1637. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7156-5-23
Amro, J., Black, C., Jemouai, Z., Rooney, N., Daneault, C., Zeytuni, N., Ruiz, M., Bui, K.H., & Baron, C. 2023. Cryo-EM structure of the Agrobacterium tumefaciens T-pilus reveals the importance of positive charges in the lumen. Structure, 31(4), .375-384. https://doi.org/10.1186/s1
Anami, S., Njuguna, E., Coussens, G., Aesaert, S., & Lijsebettens, M.V. 20132020. Higher Plant Transformation: Principles & Molecular Tools. Internationa Journal of Developed Biology, 57, 483–494. 10.1080/01904167.2013.868483
Andrieu, A., Breitler, J.C., Siré, C., Meynard, D., Gantet, P. & Guiderdoni, E. 2012. An in planta, Agrobacterium-mediated transient gene expression method for inducing gene silencing in rice (Oryza sativa L.) leaves. Rice, 5, 1-12.
Ansari, W.A., Chandanshive, S.U., Bhatt, V., Nadaf, A.B., Vats, S., Katara, J.L., Sonah, H. & Deshmukh, R. 2020. Genome editing in cereals: aroaches, alications & challenges. International Journal of Molecular Sciences, 21(11), 4040. https://doi.org/10.3390/ijms21114040
Arshad, M., & Asad, S. 2019. Embryogenic Calli Explants & Silicon Carbide Whisker-Mediated Transformation of Cotton (Gossypium hirsutum L.). Transgenic Cotton: Methods & Protocols, 75-91.
Asad, S., Mukhtar, Z., Nazir, F., Hashmi, J.A., Mansoor, S., Zafar, Y., & Arshad, M. 2008. Silicon carbide whisker-mediated embryogenic callus transformation of cotton (Gossypium hirsutum L.) & regeneration of salt tolerant plants. Molecular Biotechnology, 40, 161-169. http://www.nanoscalereslett.com/content/8/1/102
Begemann, M.B., Gray, B.N., January, E., Gordon, G.C., He, Y., Liu, H., Wu, X., Brutnell, T.P., Mockler, T.C., & Oufattole, M. 2017. PreciseInsertion & Guided Editing of Higher Plant Genomes Using Cpf1 CRISPR Nucleases. Scientific Reports, 7, 11606. https://doi.org/10.1186/s12870-023-04325-5
Belide, S., Vanhercke, T., Petrie, J.R., & Singh, S.P. 2017. Robust Genetic Transformation of Sorghum (Sorghum bicolor L.) Using Differentiating Embryogenic Callus Induced from Immature Embryos. Plant Methods, 13, 109. https://doi.org/10.1080/01904167.2022.2096467
Bian, Z., Li, S., Yang, R., Yin, J., Zhang, Y., Tu, Q., Fu, J., & Li, R. 2022. Development of a new recombineering system for Agrobacterium species. Alied & Environmental Microbiology, 88(5), .e02499-21. http://www.nanoscalereslett.com/content/8/1/102
Bonawitz, N.D., Ainley, W.M., Itaya, A., Chennareddy, S.R., Cicak, T., Effinger, K., Jiang, K., Mall, T.K., Marri, P.R., & Samuel,J.P. 2019. Zinc Finger Nuclease-mediated Targeting of Multiple Transgenes to an Endogenous Soybean Genomic Locus viaNon-homologous End Joining. Plant Biotechnology Journal, 17, 750–761. https://doi.org/10.1080/01904167.2022.2096467
Borges, F., &Martienssen, R.A. 2015. The expanding world of small RNAs in plants. Nature Reviews Molecular Cell Biology, 16(12), 727-741.
Brodersen, P. & Voinnet, O., 2006. The diversity of RNA silencing pathways in plants. Trends in Genetics, 22(5), 268-280.
Buiatti, M., Marcheschi, G., Venturo, R., Bettini, P., Bogani, P., Morpurgo, R., Nacmias, B., &Pellegrini, M.G. 1987. In vitro response to Fusarium elicitor & toxic substances in crosses between resistant & susceptible carnation cultivars. Plant Breeding, 98(4), 346-348.
Busov, V. B., Brunner, A. M., Meilan, R., Filichkin, S., Ganio, L., Gandhi, S., & Strauss, S. H. 2005. Genetic transformation: A powerful tool for dissection of adaptive traits in trees. New Phytologist, 167, 9–18. https://doi.org/10.1186/s12870-023-04325-5
Butardo, V.M., Fitzgerald, M.A., Bird, A.R., Gidley, M.J., Flanagan, B.M., Larroque, O., Resurreccion, A.P., Laidlaw, H.K., Jobling, S.A., Morell, M.K., &Rahman, S. 2011. Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA-and hairpin RNA-mediated RNA silencing. Journal of Experimental Botany, 62(14), 4927-4941.
Calabuig-Serna, A., Mir, R., Porcel, R., & Seguí-Simarro, J.M. 2023. The Highly Embryogenic Brassica napus DH4079 line is recalcitrant to Agrobacterium-mediated genetic transformation. Plants, 12(10), p.2008. https://doi.org/10.1080/01904167.2022.2096467
Carroll, D. 2011. Genome engineering with zinc-finger nucleases. Genetics, 188(4), 773-782.
Čermák, T., Baltes, N.J., Čegan, R., Zhang, Y., &Voytas, D.F. 2015. High-frequency, precise modification of the tomato genome. Genome biology, 16, 1-15.
Chilton, M.D.M., & Que, Q. 2003. Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant physiology, 133(3), 956-965. http://www.nanoscalereslett.com/content/8/1/102
Chumakov, M.I., Rozhok, N.A., Velikov, V.A., Tyrnov, V.S. & Volokhina, I.V. 2006. Agrobacterium-mediated in planta transformation of maize via pistil filaments. Russian Journal of Genetics, 42, 893-897. https://doi.org/10.1134/S1022795406080072
Crossway, A., Oakes, J.V., Irvine, J.M., Ward, B., Knauf, V.C., & Shewmaker, C.K.1986. Integration of Foreign DNA Following Microinjection of Tobacco Mesophyll Protoplasts. Molecular Gene & Genetics, 202, 179–185. https://doi.org/10.1186/s12870-023-04325-5
Das, D.K. 2018. Expression of a bacterial chitinase (ChiB) gene enhances resistance against Erysiphae polygoni induced powdery mildew disease in the transgenic black gram (Vigna mungo L.)(cv. T9). American Journal of Plant Sciences, 9(8), 1759-1770. https://doi.org/10.4236/ajps.2018.98128
Debernardi, J.M., Tricoli, D.M., Ercoli, M.F., Hayta, S., Ronald, P., Palatnik, J.F., & Dubcovsky, J. 2020. A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nature Biotechnology, 38(11), .1274-1279. https://doi.org/10.1080/01904167.2022.2096467
Desiderio, F., Zarei, L., Licciardello, S., Cheghamirza, K., Farshadfar, E., Virzi, N., Sciacca, F., Bagnaresi, P., Battaglia, R., Guerra, D., Palumbo, M., Cattivelli, L., & Mazzucotelli, E. 2019. Genomic regions from an iranian landrace increase kernel size in durum wheat. Frontier in Plant Science, 10, 448-468. http://www.nanoscalereslett.com/content/8/1/102
Du, C., Chai, L.A., Liu, C., Si, Y., & Fan, H. 2022. Improved Agrobacterium tumefaciens-mediated transformation using antibiotics & acetosyringone selection in cucumber. Plant Biotechnology Reports, 16(1), .17-27. 10.1080/01904167.2013.868483
Du, H., Shen, X., Huang, Y., Huang, M., & Zhang, Z. 2016. Overexpression of vitreoscilla hemoglobin increases waterlogging tolerance in arabidopsis & maize. BMC Plant Biology, 16, 35. https://doi.org/10.1186/s12870-021-02919-5
Duan, X., Hou, Q., Liu, G., Pang, X., Niu, Z., Wang, X., Zhang, Y., Li, B., & Liang, R. 2018. Expression of Pinellia pedatisecta lectin gene in transgenic wheat enhances resistance to wheat aphids. Molecules, 23(4), 748. http://www.nanoscalereslett.com/content/8/1/102
Elliott, C., Zhou, F., Spielmeyer, W., Panstruga, R., & Schulze-Lefert, P. 2002. Functional conservation of wheat & rice Mlo orthologs in defense modulation to the powdery mildew fungus. Molecular Plant-Microbe Interactions, 15(10), 1069-107
Fahim, M., Millar, A.A., Wood, C.C., &Larkin, P.J. 2012. Resistance to Wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnology Journal, 10(2), 150-163. https://doi.org/10.1111/j.1467-7652.2011.00647.x
Fallahi, N., Tahmasebi, Z., & Zebarjadi, A. 2022. Effect of explant, type & concentration of hormone on callus induction & regeneration of two Iranian sesame (Sesamum indicum L.) cultivars. 10.1080/01904167.2013.868483
Fllahi, N., Zebarjadi, A., & Tahmasebi, Z. 2024. Optimization of effective factors in the transfer of FAD3 gene effective in omega-3 biosynthesis to two sesame cultivars. Modern Genetics Journal, 18(4), .377-388. https://doi.org/10.1080/01904167.2022.2096467
Gao, S., Yang, Y., Wang, C., Guo, J., Zhou, D., Wu, Q., Su, Y., Xu, L., & Que, Y. 2016. Transgenic Sugarcane with a Cry1Ac Gene Exhibited Better Phenotypic Traits & Enhanced Resistance against Sugarcane Borer. PLoS ONE, 11, e0153929. https://doi.org/10.1186/s12870-023-04325-5
Gasparis, S., Kała, M., Przyborowski, M., Orczyk, W. & Nadolska-Orczyk, A. 2017. Artificial microRNA-based specific gene silencing of grain hardness genes in polyploid cereals aeared to be not stable over transgenic plant generations. Frontiers in Plant Science, 7, 2017.
Gasparis, S., Orczyk, W., &Nadolska-Orczyk, A. 2013. Sina & Sinb genes in triticale do not determine grain hardness contrary to their orthologs Pina & Pinb in wheat. BMC Plant Biology, 13, 1-12. https://doi.org/10.1186/1471-2229-13-190
Gasparis, S., Orczyk, W., Zalewski, W., & Nadolska-Orczyk, A. 2011. The RNA-mediated silencing of one of the Pin genes in allohexaploid wheat simultaneously decreases the expression of the other, & increases grain hardness. Journal of Experimental Botany, 62(11), 4025-4036. https://doi.org/10.1093/jxb/err103
Ge, X., Xu, J., Yang, Z., Yang, X., Wang, Y., Chen, Y., Wang, P., & Li, F. 2023. Efficient genotype‐independent cotton genetic transformation & genome editing. Journal of Integrative Plant Biology, 65(4), 907-917. https://doi.org/10.1186/s12870-021-02919-5
Gelvin, S.B. 2003. Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiology & Molecular Biology Reviews, 67(1), 16-37. https://doi.org/10.1128/mmbr.67.1.16-37.2003
Gil‐Humanes, J., Wang, Y., Liang, Z., Shan, Q., Ozuna, C.V., Sánchez‐León, S., Baltes, N.J., Starker, C., Barro, F., Gao, C., &Voytas, D.F. 2017. High‐efficiency gene targeting in hexaploid wheat using DNA replicons & CRISPR/Cas9. The Plant Journal, 89(6), 1251-1262. https://doi.org/10.1111/tpj.13446
Gouka, R.J., Gerk, C., Hooykaas, P.J., Bundock, P., Musters, W., Verrips, C.T., & de Groot, M.J. 1999. Transformation of Aspergillus awamori by Agrobacterium tumefaciens–mediated homologous recombination. Nature Biotechnology, 17(6), .598-601. http://www.nanoscalereslett.com/content/8/1/102
Grazziotin, M.A., Cabral, G.B., Ibrahim, A.B., Machado, R.B., & Aragão, F.J. 2020. Expression of the Arcelin 1 gene from Phaseolus vulgaris L. in cowpea seeds (Vigna unguiculata L.) confers bruchid resistance. Annals of Alied Biology, 176(3), 268-274. 10.1080/01904167.2013.868483
Hassan, M. Akram, Z. Ali, S.  Ali, G.M. Zafar, Y.  Shah, Z.H., &  Alghabari, F. 2016. Whisker-Mediated Transformation of Peanut with Chitinase Gene Enhances Resistance to Leaf Spot Disease. Crop Breeding & Alied Biotechnology, 16, 108–114. https://doi.org/10.1080/01904167.2022.2096467
Hayta, S., Smedley, M.A., Demir, S.U., Blundell, R., Hinchliffe, A., Atkinson, N., & Harwood, W.A. 2019. An efficient & reproducible Agrobacterium-mediated transformation method for hexaploid wheat (Triticum aestivum L.). Plant Methods, 15, .1-15. https://doi.org/10.1186/s12870-023-04325-5
Hensel, G., Himmelbach, A., Chen, W., Douchkov, D. K., & Kumlehn, J. 2011. Transgene expression systems in the Triticeae cereals. Journal of Plant Physiology, 168(1), 30-44.
Hensel, G., Marthe, C., & Kumlehn, J. 2017. Agrobacterium-mediated transformation of wheat using immature embryos. Wheat Biotechnology: Methods & Protocols, 129-139. http://www.nanoscalereslett.com/content/8/1/102
Himmelbach, A., Liu, L., Zierold, U., Altschmied, L., Maucher, H., Beier, F., Schützendübel, A. 2010. Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. The Plant Cell, 22(3), 937-952.
Holm, P.B., Olsen, O., Schnorf, M., Brinch-Pedersen, H., & Knudsen, S. 2000. Transformation of barley by microinjection into isolated zygote protoplasts. Transgenic Research, 9, 21-32. https://doi.org/10.1080/01904167.2022.2096467
Horsch, R.B., Fry, J.E., Hoffmann, N.L., Wallroth, M., Eichholtz, D., Rogers, S.G., & Fraley, R.T. 1985. A simple & general method for transferring genes into plants. Science, 227(4691), .1229-1231. http://www.nanoscalereslett.com/content/8/1/102
Hu, Y., Lacroix, B.,& Citovsky, V. 2021. Modulation of plant DNA damage response gene expression during Agrobacterium infection. Biochemical & biophysical research communications, 554, .7-12. 10.1080/01904167.2013.868483
ISAAA. 2020 b. Brief 55–2019: Executive Summary. https://doi.org/10.1186/s12870-023-04325-5
Jinek, M., Jiang, F., Taylor, D.W., Sternberg, S.H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S. 2014. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science,  343, 1247997. https://doi.org/10.1126/science.1247997 
Kaeler, H.F. Gu, W. Somers, D.A., & Rines, H.W.1990. Cockburn, A.F. Silicon Carbide Fiber-Mediated DNA Delivery into Plant Cells. Plant Cell Report, 9, 415–418. https://doi.org/10.1186/s12870-021-02919-5
Karmakar, S., Molla, K.A., Gayen, D., Karmakar, A., Das, K., Sarkar, S.N., Datta, K., & Datta, S.K. 2019. Development of a Rapid & Highly Efficient Agrobacterium -Mediated Transformation System for Pigeon Pea [Cajanus cajan (L.) Millsp]. GM Crops Food, 10, 115–138. https://doi.org/10.1080/01904167.2022.2096467
Karny, A., Zinger, A., Kajal, A., Shainsky-Roitman, J., & Schroeder, A. 2018. Therapeutic nanoparticles penetrate leaves & deliver nutrients to agricultural crops. Scientific Reports, 8(1), .1-10. 10.1080/01904167.2013.868483
Kaur, A., Reddy, M.S., & Kumar, A. 2022. Heat shock enhanced Agrobacterium tumefaciens mediated T-DNA delivery to potato (Solanum tuberosum L.). Journal of Plant Biochemistry & Biotechnology, 31(4), 853-863. http://www.nanoscalereslett.com/content/8/1/102
Kausch, A.P., Nelson-Vasilchik, K., Hague, J., Mookkan, M., Quemada, H., Dellaporta, S., Fragoso, C., & Zhang, Z.J. 2019. Edit atWill:Genotype Independent Plant Transformation in the Era of Advanced Genomics & Genome Editing. Plant Science, 281, 186–205. https://doi.org/10.1186/s12870-021-02919-5
Kawai, J., Kanazawa, M., Suzuki, R., Kikuchi, N., Hayakawa, Y., & Sekimoto, H. 2022. Highly efficient transformation of the model zygnematophycean alga Closterium peracerosum‐strigosum‐littorale complex by square‐pulse electroporation. New Phytologist, 233(1), .569-578. https://doi.org/10.1080/01904167.2022.2096467
Kis, A., Tholt, G., Ivanics, M., Várallyay, É., Jenes, B. & Havelda, Z. 2016. Polycistronic artificial miRNA‐mediated resistance to W heat dwarf virus in barley is highly efficient at low temperature. Molecular Plant Pathology, 17(3), .427-437.
Kluepfel, D.A., McClean, A.E., Aradhya, M.K., & Moersfelder, J.W. 2014, April. Identification of Juglans wild relatives resistant to crown gall caused by Agrobacterium tumefaciens. In II International Symposium on Wild Relatives of Subtropical & Temperate Fruit & Nutrient Crops 1074 (. 87-94). https://doi.org/10.1186/s12870-023-04325-5
Koetle, M.J., Finnie, J.F., Balázs, E., & Van Staden, J. 2015. A review on factors affecting the Agrobacterium-mediated genetic transformation in ornamental monocotyledonous geophytes. South African Journal of Botany, 98, .37-44. http://www.nanoscalereslett.com/content/8/1/102
Koornneef, M. & Meinke, D. 2010. The development of Arabidopsis as a model plant. The Plant Journal, 61(6), .909-921.
Kotnik, T., Rems, L., Tarek, M., & Miklavcic, D. 2019. Membrane Electroporation & Electropermeabilization: Mechanisms & Models. Annual Review in Biophysics, 48, 63–91. http://www.nanoscalereslett.com/content/8/1/102
Kumar, R., Mamrutha, H.M., Kaur, A., Venkatesh, K., Sharma, D., & Singh, G.P. 2019. Optimization of Agrobacterium-mediated transformation in spring bread wheat using mature & immature embryos. Molecular biology reports, 46(2), 1845-1853. 10.1080/01904167.2013.868483
Li, M., Wang, D., Long, X., Hao, Z., Lu, Y., Zhou, Y., Peng, Y., Cheng, T., Shi, J., & Chen, J. 2022. Agrobacterium-mediated genetic transformation of embryogenic callus in a Liriodendron hybrid (L. Chinense × L. Tulipifera). Frontiers in Plant Science, 13, p.802128. https://doi.org/10.1080/01904167.2022.2096467
Li, X., Yang, Q., Peng, L., Tu, H., Lee, L.Y., Gelvin, S.B., & Pan, S.Q. 2020. Agrobacterium-delivered VirE2 interacts with host nucleoporin CG1 to facilitate the nuclear import of VirE2-coated T complex. Proceedings of the National Academy of Sciences, 117(42), .26389-26397. https://doi.org/10.1186/s12870-021-02919-5
Liu, H., Zhao, J., Chen, F., Wu, Z., Tan, J., Nguyen, N.H., Cheng, Z., & Weng, Y. 2023. Improving Agrobacterium tumefaciens− mediated genetic transformation for gene function studies & mutagenesis in cucumber (Cucumis sativus L.). Genes, 14(3), p.601. https://doi.org/10.1080/01904167.2021.1963773
Liu, K., Gao, Y., Li, Z.H., Liu, M., Wang, F.Q., & Wei, D.Z. 2022. CRISPR-Cas12a assisted precise genome editing of Mycolicibacterium neoaurum. New Biotechnology, 66, .61-69. 10.1080/01904167.2013.868483 
Lorz, H., Paszkowski, J., Dierks-Ventling, C., & Potrykus, I. 1981. Isolation & Characterization of Cytoplasts & Miniprotoplasts Derived from Protoplasts of Cultured Cells. Physiology of Plant, 53, 385–391. https://doi.org/10.1186/s12870-023-04325-5
Lu, Y., Tian, Y., Shen, R., Yao, Q., Wang, M., Chen, M., Dong, J., Zhang, T., Li, F., Lei, M. & Zhu, J.K. 2020. Targeted, efficient sequence insertion & replacement in rice. Nature Biotechnology, 38(12), .1402-1407.
Lv, Q., Chen, C., Xu, Y., Hu, S., Wang, L., Sun, K., Chen, X., & Li, X. 2017. Optimization of Agrobacterium tumefaciens-mediated transformation systems in tea plant (Camellia sinensis). Horticultural Plant Journal, 3(3), 105-109. https://doi.org/10.1080/01904167.2022.2096467
Lv, Z., Jiang, R., Chen, J., & Chen, W. 2020. Nanoparticle‐mediated gene transformation strategies for plant genetic engineering. The Plant Journal, 104(4), .880-891. https://doi.org/10.1080/01904167.2021.1963773
Masani, M.Y.A., Noll, G.A., Parveez, G.K.A., Sambanthamurthi, R., & Prüfer, D. 2014. Efficient transformation of oil palm protoplasts by PEG-mediated transfection & DNA microinjection. PloS One, 9(5), p.e96831. https://doi.org/10.1186/s12870-021-02919-5
Masters, A., Kang, M., McCaw, M., Zobrist, J.D., Gordon-Kamm, W., Jones, T, & Wang, K. 2020. Agrobacterium-mediated immature embryo transformation of recalcitrant maize inbred lines using morphogenic genes. Journal of Visualized Experiments. 10(156), 60-78. https://doi.org/10.1080/01904167.2022.2096467
Melchiorre, M., Robert, G., Trii, V., Racca, R., & Lascano, H. R. 2009. Superoxide dismutase & glutathione reductase overexpression in wheat protoplast: photooxidative stress tolerance & changes in cellular redox state. Plant Growth Regulation, 57(1), 57-68.
Miroshnichenko, D., Ashin, D., Pushin, A., & Dolgov, S. 2018. Genetic transformation of einkorn (Triticum monococcum L. ssp. monococcum L.), a diploid cultivated wheat species. BMC Biotechnology, 18, 1-13. 10.1080/01904167.2013.868483
Mizuno, K., Takahashi, W., Ohyama, T., Shimada, T., & Tanaka, O. 2004. Improvement of the Aluminum Borate Whisker-Mediated Method of DNA Delivery into Rice Callus. Plant Production Science, 7, 45–49. https://doi.org/10.1080/01904167.2022.2096467
Mohanta, D., Patnaik, S., Sood, S., &Das, N. 2019. Carbon nanotubes: Evaluation of toxicity at biointerfaces. Journal of Pharmaceutical Analysis, 9(5), 293-300.
Moiseeva, Y.M., Velikov, V.A., Volokhina, I.V., Gusev, Y.S., Yakovleva, O.S. & Chumakov, M.I. 2014. Agrobacterium-mediated transformation of maize with antisense suression of the proline dehydrogenase gene by an in planta method. British Biotechnology Journal, 4, 116-125. http://www.sciencedomain.org/abstract.php?iid=364&id=11&aid=2706
 Najera VA, Twyman RM, Christou P, Zhu C. 2019. Alications of multiplex genome editing in higher plants. Current Opinion on Biotechnology, 59, 93-102, https://doi.org/10.1016/j.copbio.2019.02.015
Naseri, G., Sohani, M.M., Pourmassalehgou, A. & Allahi, S. 2012. In planta transformation of rice (Oryza sativa) using thaumatin-like protein gene for enhancing resistance to sheath blight. African Journal of Biotechnology, 11(31), .7885-7893.
National Academy of Sciences, 113, 1949–1954. 10.1080/01904167.2013.868483
Niazian, M., Noori, S.A.S., Galuszka, P., & Mortazavian, S.M.M. 2017. Tissue culture-based Agrobacterium-mediated & in Planta transformation methods. https://doi.org/10.1186/s12870-021-02919-5
Ning, W., Zhai, H., Yu, J., Liang, S., Yang, X., Xing, X., Huo, J., Pang, T., Yang, Y., & Bai, X. 2017. Overexpression of Glycine soja WRKY20 enhances drought tolerance & improves plant yields under drought stress in transgenic soybean. Molecular Breeding, 37, 1-10. https://doi.org/10.1080/01904167.2021.1963773
Ossowski, S., Schwab, R., &Weigel, D., 2008. Gene silencing in plants using artificial microRNAs & other small RNAs. The Plant Journal, 53(4), 674-690.
Ossowski,S.,Schwab,R.,andWeigel,D.(2008).Genesilencinginplantsusing  artificial micro RNA  sand other smallRNAs. Plant Journal. 53, 674–690. doi: 10.1111/ j.1365-313X.2007.03328.x
Petolino, J.F., Hopkins, N.L., Kosegi, B.D., & Skokut, M. 2000. Whisker-mediated transformation of embryogenic callus of maize. Plant Cell Reports, 19, 781-786. https://doi.org/10.1080/01904167.2022.2096467
Ramkumar, T.R.,  Lenka, S.K., Arya, S.S., & Bansal, K.C. 2020. A Short History & Perspectives on Plant Genetic Transformation. In Biolistic DNA Delivery in Plants; Rustgi, S., Luo, H., Eds.; Humana: New York, NY, USA, . 39–68. 10.1080/01904167.2013.868483
Razzaq, A., Hafiz, I.A., Mahmood, I. & Hussain, A. 2011. Development of in planta transformation protocol for wheat. African Journal of Biotechnology, 10(5), p.740.
Reddy, S.S.S., Singh, B., Peter, A.J., & Rao, T.V. 2019. Genetic transformation of indica rice varieties involving Am-SOD gene for improved abiotic stress tolerance. Saudi Journal of Biological Sciences, 26(2), 294-300. https://doi.org/10.1080/01904167.2022.2096467
Rod-In, W., Sujipuli, K. & Ratanasut, K. 2014. The floral-dip method for rice (Oryza sativa) transformation.
Rogers, K., &Chen, X., 2013. Biogenesis, turnover, & mode of action of plant microRNAs. The Plant Cell, 25(7), 2383-2399.
Saed-Moucheshi A., & Mozafari A. A. 2022. Alternate gene expression profiling of monoterpenes in Hymenocrater longiflorus as a novel pharmaceutical plant under water deficit. Scientific Reports, 12(1): 4084. 10.1080/01904167.2013.868483
Saed-Moucheshi A., & Safari H. 2023a. Investigation of regulatory elements related to superoxide dismutase enzyme genes in wheat. Cereal Biotechnology & Biochemistry, 1(3) 23-38. 10.1080/01904167.2013.868483
Saed-Moucheshi A., & Safari H. 2023b. Superoxide dismutase enzyme expression in root & shoot of triticale seedlings under drought stress conditions. Cereal Biotechnology & Biochemistry, 1: 581-595. http://www.nanoscalereslett.com/content/8/1/102
Saed-Moucheshi A., Sohrabi F., Fasihfar E., Baniasadi F., Riasat M., Mozafari A. A. 2021. Superoxide dismutase (SOD) as a selection criterion for triticale grain yield under drought stress: a comprehensive study on genomics & expression profiling, bioinformatics, heritability, & phenotypic variability. BMC Plant Biology, 21: 1-19. 10.1080/01904167.2013.868483
Saeed, T., & Shahzad, A.2016. Basic principles behind genetic transformation in plants. in biotechnological strategies for the conservation of medicinal & ornamental climbers; Shahzad, A., Sharma, S., iddiqui, S., Eds.; Springer: Cham, Switzerland, . 327–350. https://doi.org/10.1080/01904167.2022.2096467
Schiml, S., Fauser, F., & Puchta, H. 2014. The CRISPR/C as system can be used as nuclease for in planta gene targeting & as paired nickases for directed mutagenesis in A rabidopsis resulting in heritable progeny. The Plant Journal, 80(6), .1139-1150. https://doi.org/10.1111/tpj.12704
Sedeek, K.E., Mahas, A., &Mahfouz, M. 2019. Plant genome engineering for targeted improvement of crop traits. Frontiers in Plant Science, 10, 114. https://doi.org/10.3389/fpls.2019.00114
Shi, J., Gao, H., Wang, H., Lafitte, H.R., Archibald, R.L., Yang, M., Hakimi, S.M., Mo, H. & Habben, J.E. 2017. ARGOS 8 variants generated by CRISPR‐Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnology Journal, 15(2), 207-216. https://doi.org/10.1111/pbi.12603
Shimizu-Sato, S., Tsuda, K., Nosaka-Takahashi, M., Suzuki, T., Ono, S., Ta, K.N., Yoshida, Y., Nonomura, K.I., & Sato, Y. 2020. Agrobacterium-mediated genetic transformation of wild Oryza species using immature embryos. Rice, 13, 1-13. https://doi.org/10.1186/s12870-021-02919-5
Shreni Agrawal, E.R.. 2022. A review: Agrobacterium-mediated gene transformation to increase plant productivity. The Journal of Phytopharmacology, 11, p.111. 10.1080/01904167.2013.868483
Smith, R.H., 2013. Plant tissue culture: techniques & experiments. academic press. http://www.nanoscalereslett.com/content/8/1/102
Sohrabi F., & Saed-Moucheshi M. A. 2023. A review on biological roles of long non-coding RNAs (LncRNAs) in plants: A focus on cereal crops. Plant Biotechnology, 7, 56-71. https://doi.org/10.1080/01904167.2022.2096467
Sohrabi F.,& Saed-Moucheshi A. 2023. Investigation of NAD (P) H oxidase genes regulatory elements in wheat. Cereal Biotechnology & Biochemistry, 2, 98-117. 10.1080/01904167.2013.868483
Somssich, M., 2019. A short history of plant transformation. 2019(1), 1–28. https://peerj.com/preprints/27556/.
Song, C., Lu, L., Guo, Y., Xu, H., & Li, R. 2019. Efficient Agrobacterium-mediated transformation of the commercial hybrid poplar Populus Alba× Populus glandulosa Uyeki. International Journal of Molecular Sciences, 20(10), p.2594. http://www.nanoscalereslett.com/content/8/1/102
Sorokin, A.P., Ke, X.Y., Chen, D.F., & Elliott, M.C. 2000. Production of fertile transgenic wheat plants via tissue electroporation. Plant Science, 156(2), .227-233. https://doi.org/10.1186/s12870-021-02919-5
Supartana, P., Shimizu, T., Nogawa, M., Shioiri, H., Nakajima, T., Haramoto, N., Nozue, M. & Kojima, M. 2006. Development of simple & efficient in planta transformation method for wheat (Triticum aestivum L.) using Agrobacterium tumefaciens. Journal of Bioscience & Bioengineering, 102(3), .162-170.
Supartana, P., Shimizu, T., Shioiri, H., Nogawa, M., Nozue, M. & Kojima, M. 2005. Development of simple & efficient in planta transformation method for rice (Oryza sativa L.) using Agrobacterium tumefaciens. Journal of Bioscience & Bioengineering, 100(4), .391-397.
Sutradhar, M., & Mandal, N. 2023. Reasons & riddance of Agrobacterium tumefaciens overgrowth in plant transformation. Transgenic Research, 32(1), .33-52. https://doi.org/10.1080/01904167.2021.1963773
Teo, Y.L., 2022. Engineering of plasmid vectors for enhancing agrobacterium-mediated plant transformation (Doctoral Dissertation, UTAR). 10.1080/01904167.2013.868483
Thagun, C., Chuah, J.A. & Numata, K. 2019. Targeted gene delivery into various plastids mediated by clustered cell‐penetrating & chloroplast‐targeting peptides. Advanced Science, 6(23), 1902064.
Travella, S., Klimm, T.E. & Keller, B. 2006. RNA interference-based gene silencing as an efficient tool for functional genomics in hexaploid bread wheat. Plant Physiology, 142(1), .6-20.
van Wordragen, M., Shakya, R., Verkerk, R., Peytavis, R., van Kammen, A., & Zabel, P. 1997. Liposome-Mediated Transfer of YAC DNA to Tobacco Cells. Plant Molecular & Biology Report, 15, 170–178. https://doi.org/10.1080/01904167.2021.1963773
Veena, Jiang, H., Doerge, R.W., & Gelvin, S.B. 2003. Transfer of T‐DNA & Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation & suresses host defense gene expression. The Plant Journal, 35(2), .219-236. https://doi.org/10.1186/s12870-021-02919-5
Wang, M., Sun, R., Zhang, B., & Wang, Q. 2019. Pollen tube pathway-mediated cotton transformation. Transgenic Cotton: Methods & Protocols, .67-73. http://www.nanoscalereslett.com/content/8/1/102
Weeks, D.P.; Spalding, M.H.; Yang, B. 2016. Use of designer nucleases for targeted gene & genome editing in plants. Plant Biotechnology Journal, 14, 483–495. https://pubmed.ncbi.nlm.nih.gov/26261084/
Wen, S.S., Ge, X.L., Wang, R., Yang, H.F., Bai, Y.E., Guo, Y.H., Zhang, J., Lu, M.Z., Zhao, S.T., & Wang, L.Q. 2022. An efficient agrobacterium-mediated transformation method for hybrid poplar 84K (Populus alba× P. glandulosa) using calli as explants. International Journal of Molecular Sciences, 23(4), 2216. http//:www.10.1080/01904167.2013.868483
Woodward, A.W. & Bartel, B.18. Biology in bloom: a primer on the Arabidopsis thaliana model system. Genetics, 208(4), .1337-1349.
Wright, D.A., Townsend, J.A., Winfrey Jr, R.J., Irwin, P.A., Rajagopal, J., Lonosky, P.M., Hall, B.D., Jondle, M.D. & Voytas, D.F. 2005. High‐frequency homologous recombination in plants mediated by zinc‐finger nucleases. The Plant Journal, 44(4), .693-705.
Wu, H., Acanda, Y., Jia, H., Wang, N., & Zale, J. 2016. Biolistic transformation of Carrizo citrange (Citrus sinensis Osb.× Poncirus trifoliata L. Raf.). Plant Cell Reports, 35, .1955-1962. http://www.nanoscalereslett.com/content/8/1/102
Yang, A., Su, Q.,& An, L. 2009. Ovary-drip transformation: a simple method for directly generating vector-and marker-free transgenic maize (Zea mays L.) with a linear GFP cassette transformation. Planta, 229, .793-801. https://doi.org/10.1080/01904167.2022.2096467
Ye, X., Shrawat, A., Moeller, L., Rode, R., Rivlin, A., Kelm, D., Martinell, B.J., Williams, E.J., Paisley, A., Duncan, D.R., & Armstrong, C.L. 2023. Agrobacterium-mediated direct transformation of wheat mature embryos through organogenesis. Frontiers in Plant Science, 14, p.1202235. 10.1080/01904167.2013.868483
Zahedi M. B., Hooman R., & Saed-Moucheshi A. 2016. Evaluation of antioxidant enzymes, lipid peroxidation & proline content as selection criteria for grain yield under water deficit stress in barley. Journal of Alied Biological Sciences, 8: 71-78. http://www.nanoscalereslett.com/content/8/1/102
Zale, J.M., Agarwal, S., Loar, S. and Steber, C.M. 2009. Evidence for stable transformation of wheat by floral dip in Agrobacterium tumefaciens. Plant Cell Reports, 28, .903-913. http://www .DOI 10.1007/s00299-009-0696-0