Efficient and Reproducible DNA Delivery Methods for Trees Genome Editing

Yıl 2024, Cilt: 12 Sayı: 3, 96 - 113, 20.12.2024

Khola Rafique , Alvina Gul , Bengü Türkyılmaz Ünal , Volkan Altay , Münir Öztürk

https://doi.org/10.31195/ejejfs.1521281

Öz

Genome editing aimed at manipulating and improving targeted genes is widely used for the study of basic biological processes and specific improvement of desirable and novel characters in commercially important tropical as well as subtropical fruit, nuts and forest trees. The technique involves precise and accurate changing and editing of the genome through DNA insertion, deletion, or replacement via multiple genome editing tools. Trees are considered an invaluable commodity that not only provides energy, fiber and materials but also safeguards global climate and such genome editing techniques are reliable and have great potential to further improve these imperative traits and allow us to boost productivity, enhance wood quality and improve resistance to several biotic and abiotic stresses. Tree breeding is considered a lengthy procedure that often requires a few to more than 10 years due to the tree’s long juvenile phases, large size and asexual propagation nature. Traditional tree breeding strategies via conventional cross-breeding and induced mutations have led to the development of new fruit tree cultivars. However, precise tree genome editing techniques might play a valuable supplementary tool for their improvement. Over the last decade, numerous methods have been exploited for DNA delivery, such as the application of biotechnology in breeding via Agrobacterium-mediated transformation has been proven successful and possesses a huge potential with increased availability of sequenced genomes of Fruits and nuts that can be efficiently used for the improvement of the trait. Various other potential genome editing tools such as ZFNs, TALENs and most recently CRISPR/Cas9 have been effectively utilized for several fruit trees. Various improvements and alterations have been introduced worldwide to enhance the efficiency and reproducibility of the existing delivery protocols. In this review, various DNA delivery methods for genome editing together with their fundamental principles, procedures, efficacy and future prospects will be discussed.

Anahtar Kelimeler

Genome editing, DNA, Agrobacterium, CRISPR/Cas9, Trees

Kaynakça

• References Abdurakhmonov, I.Y. (2016). Genomics Era for Plants and Crop Species, Advances Made and Needed Tasks Ahead. In: Abdurakhmonov, I.Y. (Ed.), Plant Genomics InTech, Croatia, Balkans, pp. 3-16.
• Anami, S., Njuguna, E., Coussens, G., Aesaert, S., Van, Lijsebettens, M. (2013). Higher plant transformation: Principles and molecular tools. The International Journal of Developmental Biology, 57, 483-494. doi:10.1387/ijdb.130232mv
• Aradhya, M.K., Velasco, D., Wang, J.R., Ramasamy, R., You, F.M. et al. (2019). A fine-scale genetic linkage map reveals genomic regions associated with economic traits in walnut (Juglans regia L.). Plant Breeding, 138, 635-646. doi: 10.1111/pbr.12703
• Arora, L., Narula, A. (2017). Gene Editing and Crop Improvement Using CRISPR-Cas9 System. Frontiers Plant Science, 8, 1932.
• Barton, C.R., Adams, T.L., Zarovitz, M. (1991). Stable transformation of foreign DNA into Coffea arabica plants. In: Proceedings of the 14th International Conference on Coffee Science; San Francisco, USA, pp. 460-464.
• Bates, G.W. (1989). Electroporation of Protoplasts. Journal of Tissue Culture Methods, 12, 121-126.
• Becker, D.K., Dugdale, B., Smith, M.K., Harding, R.M., Dale, J.L. (2000). Genetic transformation of Cavendish banana (Musa spp. AAA group) cv ‘Grand Nain’ via microprojectile bombardment. Plant Cell Reports, 19(3), 229-234. doi: 10.1007/s002990050004
• Bespalhok, F.J.C., Kobayashi, A.K., Pereira, L.F., Galvão, R.M., Vieira, L.G. (2003). Transient gene expression of beta-glucuronidase in citrus thin epicotyl transversal sections using particle bombardment. Brazilian Archives of Biology and Technology, 46(1), 1-6. doi: 10.1590/S1516-89132003000100001
• Bewg, W.P., Ci, D., Tsai, C.J. (2018). Genome editing in trees: From multiple repair pathways to Long-Term Stability. Frontiers Plant Science, 23(9), 1732. doi: 10.3389/fpls.2018.01732.
• Borrelli, V.M.G., Brambilla, V., Rogowsky, P., Marocco, A., Lanubile, A. (2018). The enhancement of plant disease resistance using CRISPR/Cas9 technology. Frontiers Plant Science, 9, 1245.
• Breitler, J.C., Dechamp, E., Campa, C., Zebral, Rodrigues, L.A., Guyot, R. et al. (2019). CRISPR/Cas9-mediated e_cient targeted mutagenesis has the potential to accelerate the domestication of Co_ea canephora. Plant Cell Tissue Organ Culture, 134, 383-394.
• Bruegmann, T., Deecke, K., Fladung, M. (2019). Evaluating the efficiency of gRNAs in CRISPR/Cas9 mediated genome editing in poplars. International Journal of Molecular Science, 20, 3623.
• Cao, H. X., Vu, G. T. H., Gailing, O. (2022). From genome sequencing to CRISPR-based genome editing for climate-resilient forest trees. International Journal of Molecular Sciences, 23(2), 966.
• Cardi, T., Murovec, J., Bakhsh, A., Boniecka, J., Bruegmann, T., Bull, S. E., ... & Van Laere, K. (2023). CRISPR/Cas-mediated plant genome editing: outstanding challenges a decade after implementation. Trends in Plant Science, 28(10), 1144-1165.
• Carlson, D.F., Fahrenkrug, S.C., Hackett, P.B. (2012). Targeting DNA with fingers and TALENs. Molecular Therapy-Nucleic Acids, 1, 1.
• Carroll, D., Morton, J.J., Beumer, K.J., Segal, D.J. (2006). Design, construction and in vitro testing of zinc finger nucleases. Nature Protocols, 1, 1329-1341.
• Charity, J.A., Holland, L., Grace, L.J., Walter, C. (2005). Consistent and stable expression of the nptII, uidA and bar genes in transgenic Pinus radiata after Agrobacterium-mediated transformation using nurse cultures. Plant Cell Reports, 23, 606-616.
• Charrier, A., Vergne, E., Dousset, N.J.P., Richer, A., Petiteau, A. et al. (2019). Efficient targeted mutagenesis in apple and first time edition of pear using the CRISPR-Cas9 system. Frontiers in Plant Science, 10, 40.
• Chee, W.W., Jalil, M., Abdullah, M.O., Othman, R.Y., Khalid, N. (2005). Comparison of beta-glucuronidase expression and anatomical localization in bombarded immature embryos of banana cultivar mas via biolistic transformation. Asia-Pacific Journal of Molecular Biology and Biotechnology, 13 (1), 15-22.
• Chen, K., Wang, Y., Zhang, R., Zhang, H., Gao, C. (2019). CRISPR/Cas genome editing and precision plant breeding in agriculture. Annual Review of Plant Biology, 70, 667-697. doi: 10.1146/annurev-arplant-050718-100049
• Chen, Q., Lai, H. (2015). Gene delivery into plant cells for recombinant protein production. BioMed Research international 17, 2015.
• Chutyser, W., Renders, T., Van Den Bosch, S., Koelewijn, S-F., Beckham, G.T. et al. (2018). Chemicals from lignin: an interplay of lignocellulose fractionation, depolymerisation, and upgrading. Chemical Society Reviews, 47, 852-908.
• Corte, L.E.D., Mahmoud, L.M., Moraes, T.S., Mou, Z., Grosser, J.W. and Dutt, M. (2019). Development of Improved Fruit, Vegetable, and Ornamental Crops Using the CRISPR/Cas9 Genome Editing Technique. Plants, 8, 601. doi:10.3390/plants8120601
• Dai, Y., Hu, G., Dupas, A., Medina, L., Blandels, N. et al. (2020). Implementing the CRISPR/Cas9 Technology in Eucalyptus Hairy Roots Using Wood-Related Genes. International Journal of Molecular Sciences, 21(10), 3408.
• Davies, H.M. (2010). Commercialization of whole-plant systems for biomanufacturing of protein products: evolution and prospects. Plant Biotechnology Journal, 8(8), 845-861.
• Dönmez, D., Şimşek, Ö., Kaçar, Y.A. (2016). Genetic engineering techniques in fruit science. International Journal of Environmental & Agriculture Research (IJOEAR), 2(12), 115-128.
• Donmez, D., Şimsek, O., Aka Kacar, Y. (2016). Genetic Engineering Techniques in Fruit Science. International Journal of Environmental and Agriculture Research (IJOEAR), 2(12), 115-128.
• Doudna, J.A., Charpentier, E. (2014). Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science, 28(346), 6213. doi: 10.1126/science.1258096. PMID: 25430774
• Durai, S., Mani, M., Kandavelou, K., Wu, J., Porteus, M.H. et al. (2005). Zinc finger nucleases: Custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Research, 33, 5978-5990.
• Elorriaga, E., Klocko, A.L., Ma, C., Strauss, S.H. (2018). Variation in mutation spectra among CRISPR/Cas9 mutagenized poplars. Frontiers Plant Science, 9, 594.
• Endo, S., Matsunaga, E., Yamada-Watanabe, K., Ebinuma, H. (2002). Application of Genetic Engineering for Forest Tree Species. In: Omasa, K., Saji, H., Youssefian, S., Kondo, N. (Eds). Air Pollution and Plant Biotechnology. Tokyo, Springer. https://doi.org/10.1007/978-4-431-68388-9_22
• Fan, D., Liu, T., Li, C., Jiao, B., Li, S. et al. (2015). Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports, 5, 12217.
• Fillatti, J.J., Sellmer, J., McCown, B., Haissig, B., Comai, L. (1987). Agrobacterium-mediated transformation and regeneration of Populus. Molecular and General Genetics, 206, 192-199.
• Fiore, A., Lardo, E., Montanaro, G., Laterza, D., Loiudice, C. et al. (2018). Mitigation of global warming impact of fresh fruit production through climate smart management. Journal of Cleaner Production, 172, 3634-3643. doi: 10.1016/j.jclepro.2017.08.062
• Fister, A.S., Landherr, L., Maximova, S.N., Guiltinan, M.J. (2018). Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in Theobroma cacao. Frontiers in Plant Science, 9, 268.
• Fladung, M., Kumar, S., Ahuja, M.R. (1997). Genetic transformation of Populus genotypes with different chimeric gene constructs: transformation efficiency and molecular analysis. Transgenic Research, 6, 111121.
• Franks, T., He, D.G., Thomas, M. (1998). Regeneration of Transgenic Shape Vitis vinifera L. Sultana Plants: Genotypic and Phenotypic Analysis. Molecular Breeding, 4(4), 321-333.
• Gaj, T., Gersbach, C.A., Barbas, C.F. (2013). ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 31, 397-405.
• Gelvin, S.B. (2003). Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiology and Molecular Biology Reviews Journal, 67 (1), 16-37.
• Harfouche, A., Meilan, R., Altman, A. (2011). Tree genetic engineering and applications to sustainable forestry and biomass production. Trends in Biotechnology, 29 (1), 9-17.
• Henderson, A.R., Walter, C. (2006). Genetic engineering in conifer plantation forestry. Silvae Genetica, 55, 253-262.
• Holland, L., Gemmell, J.E., Cl, J.A., Walter, C. (1997). Foreign gene transfer into Pinus radiata cotyledons by Agrobacterium tumefaciens. New Zealand Journal of Forestry Science, 27, 289-304.
• Houllou-Kido, L.M., Kido, E.A., Falco, M.C., Silva Filho, M.D.C., Figueira, A.V.D.O. et al. (2005). Somatic embryogenesis and the effect of particle bombardment on banana Maçã regeneration. Pesquisa Agropecuária Brasileira, 40(11), 1081-1086. doi: 10.1590/S0100-204X2005001100005
• Huang, Y., Diner, A.M., Karnosky, D.F. (1991). Agrobacterium rhizogenes mediated genetic transformation and regeneration of a conifer: Larix decidua. In vitro Cellular & Developmental Biology–Plant, 27, 201-207.
• Jaganathan, D., Ramasamy, K., Sellamuthu, G., Jayabalan, S., Venkataraman, G. (2018). CRISPR for crop improvement: an update review. Frontiers in Plant Science, 17 (9), 985.
• Jia, H., Wang, N. (2014a). Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One, 9,e93806.
• Jia, H., Wang, N. (2014b). Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Reports, 33, 1993-2001.
• Jia, H., Xu, J., Orbovi´c, V., Zhang, Y., Wang, N. (2017). Editing Citrus Genome via SaCas9/sgRNA System. Frontiers in Plant Science, 8, 2135.
• Jiang, Y., Guo, L., Ma, X., Zhao, X., Jiao, B. et al. (2017). The WRKY transcription factors PtrWRKY18 and PtrWRKY35 promote Melampsora resistance in Populus. Tree Physiology, 37, 665-675.
• Kamburova ,V.S., Nikitina, E.V., Shermatov, S.E., Buriev, Z.T., Kumpatla, S.P. (2017). Genome editing in plants: an overview of tools and applications. International Journal of Agronomy, 10, 2017.
• Kaur, N., Alok, A., Shivani, N., Kaur, N., Pandey, P. (2018). CRISPR/Cas9-mediated efficient editing in phytoene desaturase (PDS) demonstrates precise manipulation in banana cv. Rasthali genome. Functional and Integrative Genomics, 18, 89-99.
• Keshavareddy, G., Kumar, A.R.V., Vemanna, S.R. (2018). Methods of plant transformation-A review. International Journal of Current Microbiology and Applied Sciences, 7 (7), 2656-2668. doi: 10.20546/ijcmas.2018.707.312
• Klimaszewska, K., Lachance, D., Pelletier, G., Lelu, A.M., Seguin, A. 2001. Regeneration of transgenic Picea glauca, P. mariana and P. abies after co-cultivation of embryogenic tissue with Agrobacterium tumefaciens. In vitro Cellular & Developmental Biology–Plant, 37 (6), 748-755.
• Klopfenstein, N.B., McNabb, H.S. Jr, Hart, E.R., Hanna, R.D., Heuchelin, S.A. (1993). Transformation of Populus hybrids to study and improve pest resistance, Silvae Genetica, 42, 86-90.
• Le, V.Q., Belles-Isles, J., Dusabenyagasani, M., Tremlay, F.M. (2001). An improved procedure for production of white spruce (Picea glauca) transgenic plants using Agrobacterium tumefaciens. Journal of Experimental Botany, 364, 2089–2095.
• Litz, R.E., Padilla, G. (2012). Genetic transformation of fruit trees. In: Schnell R, Priyadarshan P, editors. Genomics of Tree Crops. New York, NY: Springer. DOI: 10.1007/978-1-4614-0920-5_5
• Liu, Y., Yang, H., Sakanishi, A. (2006). Ultrasound: mechanical gene transfer into plant cells by sonoporation. Biotechnology Advances, 24 (1), 1-16.
• Li M., Li, H., Jiang, H., Pan, X., Wu, G. (2008). Establishment of An Agrobacteriuim-mediated Cotyledon Disc Transformation Method for Jatropha Curcas. Plant Cell Tissue and Organ Culture. 92(2), 173-181.
• Maeder, M. L., Gersbach, C. A. (2016). Genome-editing technologies for gene and cell therapy. Molecular Therapy, 24(3), 430-446.
• Minczuk, M., Papworth, M.A., Miller, J.C., Murphy, M.P., Klug, A. (2008). Development of a single-chain, quasi-dimeric zinc-finger nuclease for the selective degradation of mutated human mitochondrial DNA. Nucleic Acids Research, 36, 3926-3938.
• Mousavi, M., Fard, M.B. (2019).Genetic Improvement of Tropical and Subtropical Fruit Trees via Biolistic Methods. InTransgenic Crops-Emerging Trends and Future Perspectives 2019 Oct 23. IntechOpen.
• Mousavi, M., Mousavi, A., Habashi, A.A., Arzani, K. (2007). Investigation on ability of date palm gene transformation. In: Proceedings of 5th Iranian Horticultural Sciences Congress. Iran: Shiraz University, p. 244.
• Kuzmanović, N., Puławska, J., Prokić, A., Ivanović, M., Zlatković, N., Jones, J.B., Obradović, A. (2015). Agrobacterium arsenijevicii sp. nov., Isolated from Crown Gall Tumors on Raspberry and Cherry Plum. Systematic and Applied Microbiology. 38(6), 373-378.
• Naim, F., Dugdale, B., Kleidon, J., Brinin, A., Shand, K., Waterhouse, P., Dale, J. (2018). Gene editing the phytoene desaturase alleles of Cavendish banana using CRISPR/Cas9. Transgenic Research, 27, 451-460.
• Nilsson, O., Moritz, T., Sundberg, B., Sandberg, G., Olsson, O. (1996). Expression of the Agrobacterium rhizogenes rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiology, 112, 493-502.
• Nishitani, C., Hirai, N., Komori, S., Wada, M., Okada, K., Osakabe, K., Yamamoto, T., Osakabe, Y. (2016). Efficient genome editing in apple using a CRISPR/Cas9 system. Scientific Reports, 6, 31481.
• Noman, A., Aqeel, M., He, S. (2016). CRISPR-Cas9: tool for qualitative and quantitative plant genome editing. Frontiers in plant science, 21(7), 1740.
• Oliveira, D. M., Cesarino, I. (2024). Genome editing of wood for sustainable pulping. Trends in Plant Science, 29(2), 111-113.
• Osakabe, Y., Osakabe, K. (2015). Genome editing with engineered nucleases in plants. Plant and Cell Physiology, 56,389-400.
• Osakabe, Y., Sugano, S.S., Osakabe, K. (2016). Genome engineering of woody plants: past, present and future. Journal of Wood Science, 62(3),217-25.
• Papworth, M., Kolasinska, P., Minczuk, M. (2006). Designer zinc-finger proteins and their applications. Gene, 366, 27-38.
• Peer, R., Rivlin, G., Golobovitch, S., Lapidot, M., Gal-On, A., Vainstein, A., Tzfira, T., Flaishman, M.A. (2015). Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta, 241, 941-951.
• Peng, A., Chen, S., Lei, T., Xu, L., He, Y., Wu, L., Yao, L. et al. (2017). Engineering canker‐resistant plants through CRISPR/Cas9‐targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnology Journal, 15, 1509-1519.
• Sauer, N.J., Mozoruk, J., Miller, R.B. et al. (2016). Oligonucleotide-directed mutagenesis for precision gene editing. Plant Biotechnology Journal, 14(2), 496-502.
• Qin, G., Gu, H., Ma, L., Peng, Y., Deng, X.W., Chen, Z., Qu, L.J. (2007). Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Research, 17, 471-482.
• Rashid, A.H.A., Lateef, D.D. (2016). Novel techniques for gene delivery into plants and its applications for disease resistance in crops. American Journal of Plant Sciences. 7,181-193. DOI: 10.4236/ajps.2016.71019
• Rivera, A.L., Gómez-Lim, M., Fernández, F., Loske, A.M. (2012). Physical methods for genetic plant transformation. Physics of Life Reviews, 9(3), 308-345. doi.org/10.1016/j.plrev.2012.06.002
• Dhekney, S.A., Li, Z.T., Zimmerman, T.W., Gray, D.J. (2009). Factors Influencing Genetic Transformation and Plant Regeneration of Vitis. American Journal of Enology and Viticulture, 60(3), 285-292.
• Ochatt, S.J., Chand, P.K, Rech, E.L., Davey, M.R., Power, J.B. (1988). Electroporation-Mediated Improvement of Plant Regeneration from Colt Cherry (Prunus avium × pseudocerasus) Protoplasts. Plant Science, 54, 165-169. Sanford, J.C. (1990). Biolistic plant transformation. Acta Physiologiae Plantarum, 79 (1), 206-209.
• Sawahel, W.A. (2002). The Production of Transgenic Potato Plants Expressing Human Alpha-İnterferon Using Lipofectin-Mediated Transformation. Cellular and Molecular Biology Letters, 7 (1), 19-30.
• Schiemann, J., Robienski, J., Schleissing, S., Spök, A., Sprink, T., Wilhelm, R.A. (2020). Editorial: Plant Genome Editing – Policies and Governance. Frontiers Plant Science, 11, 284
• Shen, Y., Li, Y., Xu, D., Yang, C., Li, C., Luo, K. (2018). Molecular cloning and characterization of a brassinosteriod biosynthesis-related gene PtoDWF4 from Populus tomentosa. Tree Physiology, 38, 1424-1436.
• Song, G.Q., Prieto, H., Orbovic, V. (2019). Agrobacterium-Mediated Transformation of Tree Fruit Crops: Methods, Progress, and Challenges. Frontiers Plant Science, 10,226. doi: 10.3389/fpls.2019.00226. PMID: 30881368; PMCID: PMC6405644.
• Sowers, A.E. (1992). Mechanisms of Electroporation and Electrofusion. In: Chang DC, Chassy, B.M., Saunders, J.A., Sowers, A.E. (Eds). Guide to Electroporation and Electrofusion, San Diego, USA: Academic Press, pp. 119-138.
• Subramaniam, S., Mahmood, M., Meon, S., Rathinam, X. (2010). Genetic engineering for tolerance to Fusarium wilt race 1 in Musa sapientum cv. Rastali (AAB) using biolistic gun transformation system. Tree and Forestry Science and Biotechnology. 4(2), 65-75.
• Tachibana, K., Uchida, T., Ogawa, K., Yamashita, N., Tamura, K. (1999). Induction of Cell-Membrane Porosity by Ultrasound. Lancet, 353 (9162), 1409.
• Tanuja, P., Kumar, A.L. (2017). Transgenic fruit crops—A review. International Journal of Current Microbiology and Applied Sciences. 6(8), 2030-2037. DOI: 10.20546/ijcmas.2017.608.241
• Tassy, C., Partier, A., Beckert, M., Feuillet, C., Barret, P. (2014). Biolistic Transformation of Wheat: İncreased Production of Plants with Simple Insertions and Heritable Transgene Expression. Plant Cell, Tissue and Organ Culture, 119 (1), 171-181.
• Thapliyal, G., Bhandari, M. S., Vemanna, R. S., Pandey, S., Meena, R. K., Barthwal, S. (2023). Engineering traits through CRISPR/cas genome editing in woody species to improve forest diversity and yield. Critical Reviews in Biotechnology, 43(6), 884-903.
• Torregrosa, L., Iocco, P., Thomas, M.R. (2002). Influence of Agrobacterium Strain, Culture Medium, and Cultivar on The Transformation Efficiency of Vitis vinifera L. American Journal of Enology and Viticulture , 53(3), 183-190.
• Tsai, C.-J., Xue, L.-J. (2015). CRISPRing into the woods. GM Crops Food, 6, 206-215.
• Tzfira, T., Jensen, C.S., Vainstein, A., Altman, A. (1997). Agrobacterium tumefaciens-mediated transformation of Populus tremula L. through direct shoot regeneration from stem segments. Physiologia Plantarum, 99, 554-561.
• Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., Gregory, P.D. (2010). Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics, 11, 636-646.
• Verma, S.R., Dwivedi, U.N. (2014). Lignin genetic engineering for improvement of wood quality: applications in paper and textile industries, fodder and bioenergy production. South African Journal of Botany, 91, 107-125.
• Vishnevetsky, J., White, T.L., Palmateer, A.J., Flaishman, M., Cohen, Y. et al. (2011). Improved tolerance toward fungal diseases in transgenic Cavendish banana (Musa spp. AAA group) cv. Grand Nain. Transgenic Research, 20 (1), 61-72. doi: 10.1007/s11248-010-93927
• Vladimir, O. (2019). Editorial: New Developments in Agrobacterium-Mediated Transformation of Tree Fruit Crops. Frontiers in Plant Science, 10, 1253.
• Walawage, S.L., Zaini, P.A., Mubarik, M.S., Martinelli, F., Balan, et al. (2019). Deploying Genome Editing Tools for Dissecting the Biology of Nut Trees. Frontiers in Sustainable Food Systems, 3, 100.
• Wan, S., Li, C., Ma, X., Luo, K. (2017). PtrMYB57 contributes to the negative regulation of anthocyanin and proanthocyanidin biosynthesis in poplar. Plant Cell Reports, 36, 1263-1276.
• Wang, H., La Russa, M., Qi, L.S. (2016). CRISPR/Cas9 in Genome Editing and Beyond. Annual Review of Biochemistry, 85, 227-64.
• Wang, L., Ran, L., Hou, Y., Tian, Q., Li, C. et al. (2017). The transcription factor MYB115 contributes to the regulation of proanthocyanidin biosynthesis and enhances fungal resistance in poplar. New Phytologist, 215, 351-367.
• Wang, W., Pan, Q., He, F., Akhunova, A., Chao, S., Trick, H., Akhunov, E. (2018). Transgenerational CRISPR-Cas9 activity facilitates multiplex gene editing in allopolyploid wheat. The CRISPR Journal, 1, 65-74.
• Wojcik, A., Rybczynski, J.J. (2015). Electroporation and Morphogenic Potential of Gentiana kurroo (Royle) Embryogenic Cell Suspension Protoplasts. BioTechnologia, 96 (1), 19-29.
• Wu, H., Acanda, Y., Jia, H., Wang, N., Zale, J. (2016). Biolistic Transformation of Carrizo Citrange (Citrus sinensis Osb. X Poncirus trifoliata L. Raf.). Plant Cell Reports, 35(9), 1955-1962.
• 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(9), 1955-1962. doi: 10.1007/s00299-016-2010-2
• Yang, L., Zhao, X., Ran, L., Li, C., Fan, D. et al. (2017). PtoMYB156 is involved in negative regulation of phenylpropanoid metabolism and secondary cell wall biosynthesis during wood formation in poplar. Scientific Reports, 7, 41209.
• Zaidi, S.S.A., Mansoor, S. (2017). Viral Vectors for Plant Genome Engineering. Frontiers in Plant Science, 8, 539.
• Zhang, F., LeBlanc, C., Irish, V.F., Jacob, Y. (2017). Rapid and efficient CRISPR/Cas9 gene editing in Citrus using the YAO promoter. Plant Cell Reports, 36, 1883-1887.
• Zhang, Y., Malzahn, A.A., Sretenovic, S., Qi, Y. (2019). The emerging and uncultivated potential of CRISPR technology in plant science. Nature Plants, 5, 778-794. doi: 10.1038/s41477-019-0461-5
• Zhou, X., Jacobs, T.B., Xue, L.J., Harding, S.A., Tsai, C.J. (2015). Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytologist, 208, 298-301.
• Zhou, Q., Dai, L., Cheng, S., He, J., Wang, D., Zhang, J., Wang, Y.A. (2014). Circulatory System Useful Both for Long-Term Somatic Embryogenesis and Genetic Transformation in Vitis vinifera L. cv. Thompson Seedless. Plant Cell, Tissue and Organ Culture, 118(1), 157-168, 2014.
• Zhu, C., Zheng, X., Huang, Y., Ye, J., Chen, P. et al. (2019). Genome sequencing and CRISPR/Cas9 gene editing of an early flowering Mini-Citrus (Fortunella hindsii). Plant Biotechnology Journal, 11(17), 2199-2210.