Genome Editing Technologies towards Tomato Improvement: Recent Advances and Future Perspectives

Sonu Priya Sahu; Raj Kumar Joshi; Rukmini Mishra

doi:10.18006/2024.12(4).537.556

Authors

Sonu Priya Sahu Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India https://orcid.org/0009-0005-8226-6797
Raj Kumar Joshi Department of Biotechnology, Rama Devi Women's University, Bhubaneswar, 751022, Odisha, India https://orcid.org/0000-0003-0505-2881
Rukmini Mishra Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India https://orcid.org/0000-0001-9692-212X

DOI:

https://doi.org/10.18006/2024.12(4).537.556

Keywords:

Solanum lycopersicon, CRISPR/Cas, Tomato breeding, Prime editing, Base editing, PAM less editing, Multiplex editing

Abstract

Tomato (Solanum lycopersicon L.) is the world's second major vegetable crop and a superior model plant for studies on fruit biology. However, the changing climatic conditions are hugely impacting the yield and quality of tomato. CRISPR/Cas9 technology has been widely used in tomato breeding for enhanced disease resistance, herbicide tolerance, domestication and urban farming of wild tomato, and improved fruit yield and quality. Furthermore, new and advanced editing systems like Cas12a, Cas12b, base editing, and prime editing have been recently applied for high-precision tomato improvement. CRISPR variants, PAM-less genome editing, advanced transformation protocols, and gene delivery systems have played a critical role in fast breeding. This review offers an informative summary of recent progress in various genome editing methods and applications for improving tomatoes. It also focuses on critical issues, regulatory concerns, and prospects of genome editing platforms to improve tomato and allied crops.

Author Biographies

Sonu Priya Sahu, Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India

Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India

Raj Kumar Joshi, Department of Biotechnology, Rama Devi Women's University, Bhubaneswar, 751022, Odisha, India

Department of Biotechnology, Rama Devi Women's University, Bhubaneswar, 751022, Odisha, India

Rukmini Mishra, Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India

Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India

References

Acevedo‐Garcia, J., Kusch, S., & Panstruga, R. (2014). Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytologist, 204(2), 273-281.

Agustin, Z., Tomas, C., Rezende, N. E., & Morato, N. M. (2018). Edel Kai H, Weinl Stefan, Freschi Luciano, Voytas Daniel F, Kudla Jörg, Peres Lázaro Eustáquio Pereira. De novo domestication of wild tomato using genome editing. Nature Biotechnology, 36(12), 1211-1216.

Ahmar, S., Saeed, S., Khan, M. H. U., Ullah Khan, S., Mora-Poblete, F., et al. (2020). A revolution toward gene-editing technology and its application to cropimprovement. International Journal of Molecular Sciences, 21(16), 5665.

Alamgir, A. N. M. (2018). Vitamins, nutraceuticals, food additives, enzymes, anesthetic aids, and cosmetics. In A. N. M. Alamgir (Ed.) Therapeutic Use of Medicinal Plants and their Extracts: Volume 2: Phytochemistry and Bioactive Compounds (pp. 407-534). Springer, Cham. https://doi.org/10.1007/978-3-319-92387-1_5.

Anzalone, A. V., Koblan, L. W., & Liu, D. R. (2020). Genome editing with CRISPR–Cas nucleases, base editors, transposases, and prime editors. Nature Biotechnology, 38(7), 824-844.

Anzalone, A. V., Zairis, S., Lin, A. J., Rabadan, R., & Cornish, V. W. (2019). Interrogation of eukaryotic stop codon readthrough signals by in vitro RNA selection. Biochemistry, 58(8), 1167-1178.

Asmamaw, M., & Zawdie, B. (2021). Mechanism and Applications of CRISPR/Cas-9-Mediated Genome Editing. Biologics : targets & therapy, 15, 353–361. https://doi.org/10.2147/BTT.S326422.

Atarashi, H., Jayasinghe, W. H., Kwon, J., Kim, H., Taninaka, Y., Igarashi, M., Ito, K., Yamada, T., Masuta, C., & Nakahara, K. S. (2020). Artificially Edited Alleles of the Eukaryotic Translation Initiation Factor 4E1 Gene Differentially Reduce Susceptibility to Cucumber Mosaic Virus and Potato Virus Y in Tomato. Frontiers in microbiology, 11, 564310. https://doi.org/10.3389/fmicb.2020.564310

Bachtiar, V., Near, J., Johansen-Berg, H., & Stagg, C. J. (2015). Modulation of GABA and resting state functional connectivity by transcranial direct current stimulation. eLife, 4, e08789. https://doi.org/10.7554/eLife.08789.

Bari, V. K., Nassar, J. A., & Aly, R. (2021a). CRISPR/Cas9 mediated mutagenesis of MORE AXILLARY GROWTH 1 in tomato confers resistance to root parasitic weed Phelipanche aegyptiaca. Scientific reports, 11(1), 3905. https://doi.org/10.1038/ s41598-021-82897-8.

Bari, V. K., Nassar, J. A., Kheredin, S. M., Gal-On, A., Ron, M., et al. (2019). CRISPR/Cas9-mediated mutagenesis of CAROTENOID CLEAVAGE DIOXYGENASE 8 in tomato provides resistance against the parasitic weed Phelipanche aegyptiaca. Scientific Reports, 9(1), 11438.

Bari, V. K., Nassar, J. A., Meir, A., & Aly, R. (2021b). Targeted mutagenesis of two homologous ATP-binding cassette subfamily G (ABCG) genes in tomato confers resistance to parasitic weed Phelipanche aegyptiaca. Journal of Plant Research, 134(3), 585-597.

Bouzroud, S., Fahr, M., Bendaou, N., Bouzayen, M., Zouine, M., et al. (2018). SlARF4 Under Expression Improves Tolerance to Salinity in Tomato (Solanum lycopersicum). International Journal of Agricultural and Natural Sciences, 1(3), 242-244.

Brooks, C., Nekrasov, V., Lippman, Z. B., Van Eck, J. (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant physiology, 166(3), 1292-1297.

Butt, H., Rao, G. S., Sedeek, K., Aman, R., Kamel, R., et al. (2020). Engineering herbicide resistance via prime editing in rice. Plant Biotechnology Journal, 18(12), 2370.

Castañeda, L., Giménez, E., Pineda, B., García-Sogo, B., Ortiz-Atienza, A., et al. (2022). Tomato CRABS CLAW paralogues interact with chromatin remodelling factors to mediate carpel development and floral determinacy. The New phytologist, 234(3), 1059–1074. https://doi.org/10.1111/nph.18034.

Cha, J. Y., Uddin, S., Macoy, D. M., Shin, G. I., Jeong, S. Y., et al. (2023). Nucleoredoxin gene SINRX1 negatively regulates tomato immunity by activating SA signaling pathway. Plant Physiology and Biochemistry, 200, 107804.

Chaudhry, S., & Sidhu, G. P. S. (2022). Climate change regulated abiotic stress mechanisms in plants: A comprehensive review. Plant Cell Reports, 41(1), 1-31.

Chen, L., Yang, D., Zhang, Y., Wu, L., Zhang, Y., et al. (2018). Evidence for a specific and critical role of mitogen‐activated protein kinase 20 in uni‐to‐binucleate transition of microgametogenesis in tomato. New Phytologist, 219(1), 176-194.

Chen, M., Zhu, X., Liu, X., Wu, C., Yu, C., et al. (2021a). Knockout of auxin response factor SlARF4 improves tomato resistance to water deficit. International Journal of Molecular Sciences, 22(7), 3347.

Chen, T., Cohen, D., Itkin, M., Malitsky, S., & Fluhr, R. (2021b). Lipoxygenase functions in 1O2 production during root responses to osmotic stress. Plant Physiology, 185(4), 1638-1651.

Cody, W. B., & Scholthof, H. B. (2019). Plant virus vectors 3.0: transitioning into synthetic genomics. Annual Review of Phytopathology, 57, 211-230.

D’Ambrosio, C., Stigliani, A. L., & Giorio, G. (2018). CRISPR/Cas9 editing of carotenoid genes in tomato. Transgenic research, 27(4), 367-378.

Dahan‐Meir, T., Filler‐Hayut, S., Melamed‐Bessudo, C., Bocobza, S., Czosnek, H., et al. (2018). Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. The Plant Journal, 95(1), 5-16.

Debbarma, J., Saikia, B., Singha, D. L., Das, D., Keot, A. K., et al. (2023). CRISPR/cas9-mediated mutation in XSP10 and slSAMT genes impart genetic tolerance to fusarium wilt disease of tomato (Solanum lycopersicum L.). Genes, 14(2), 488.

Debbarma, J., Saikia, B., Singha, D. L., Maharana, J., Velmuruagan, N., et al. (2021). XSP10 and SlSAMT, Fusarium wilt disease responsive genes of tomato (Solanum lycopersicum L.) express tissue specifically and interact with each other at cytoplasm in vivo. Physiology and Molecular Biology of Plants, 27(7), 1559-1575.

Deng, L., Wang, H., Sun, C., Li, Q., Jiang, H., et al. (2018). Efficient generation of pink-fruited tomatoes using CRISPR/Cas9 system. Journal of Genetics and Genomics= Yi chuanxue bao, 45(1), 51-54.

Do, J. H., Park, S. Y., Park, S. H., Kim, H. M., Ma, S. H., et al. (2022). Development of a genome-edited tomato with high ascorbate content during later stage of fruit ripening through mutation of SlAPX4. Frontiers in Plant Science, 13, 836916.

Dong, R., Yuan, Y., Liu, Z., Sun, S., Wang, H., et al. (2023). ASYMMETRIC LEAVES 2 and ASYMMETRIC LEAVES 2‐LIKE are partially redundant genes and essential for fruit development in tomato. The Plant Journal, 114(6), 1285-1300.

Eid, A., Alshareef, S., & Mahfouz, M. M. (2018). CRISPR base editors: genome editing without double-stranded breaks. Biochemical Journal, 475(11), 1955-1964.

Ellison, E. E., Nagalakshmi, U., Gamo, M. E., Huang, P. J., Dinesh-Kumar, S., et al. (2020). Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs. Nature plants, 6(6), 620-624.

Endo, A., Masafumi, M., Kaya, H., & Toki, S. (2016). Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisellanovicida. Scientific Reports, 6(1), 38169.

Endo, M., Mikami, M., Endo, A., Kaya, H., Itoh, T., et al. (2019). Genome editing in plants by engineered CRISPR–Cas9 recognizing NG PAM. Nature Plants, 5(1), 14-17.

Feng, Y., Kou, X., Yuan, S., Wu, C., Zhao, X., et al. (2023). CRISPR/Cas9-mediated SNAC9 mutants reveal the positive regulation of tomato ripening by SNAC9 and the mechanism of carotenoid metabolism regulation. Horticulture Research, 10(4), uhad019.

Gao, Y., Wei, W., Fan, Z., Zhao, X., Zhang, Y., et al. (2020). Re-evaluation of the nor mutation and the role of the NAC-NOR transcription factor in tomato fruit ripening. Journal of Experimental Botany, 71(12), 3560-3574.

García-Murillo, L., Valencia-Lozano, E., Priego-Ranero, N. A., Cabrera-Ponce, J. L., Duarte-Aké, F. P., et al. (2023). CRISPRa-mediated transcriptional activation of the SlPR-1 gene in edited tomato plants. Plant Science, 329, 111617.

Gaudelli, N. M., Komor, A. C., Rees, H. A., Packer, M. S., Badran, A. H., et al. (2017). Programmable base editing of A• T to G• C in genomic DNA without DNA cleavage. Nature, 551(7681), 464-471.

Gupta, S. K., Sharma, M., & Mukherjee, S. (2022). Buckeye rot of tomato in India: Present status, challenges, and future research perspectives. Plant Disease, 106(4), 1085-1095.

Hong, Y., Meng, J., He, X., Zhang, Y., Liu, Y., et al. (2021). Editing miR482b and miR482c simultaneously by CRISPR/Cas9 enhanced tomato resistance to Phytophthora infestans. Phytopathology, 111(6), 1008-1016.

Hu, G., Wang, K., Huang, B., Mila, I., Frasse, P., et al. (2022). The auxin-responsive transcription factor SlDOF9 regulates inflorescence and flower development in tomato. Nature Plants, 8(4), 419-433.

Hu, J., Israeli, A., Ori, N., & Sun, T. P. (2018). The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato. The Plant Cell, 30(8), 1710-1728.

Hu, J., Li, S., Li, Z., Li, H., Song, W., et al. (2019). A barley stripe mosaic virus‐based guide RNA delivery system for targeted mutagenesis in wheat and maize. Molecular Plant Pathology, 20(10), 1463-1474.

Hua, K., Jiang, Y., Tao, X., & Zhu, J. K. (2020). Precision genome engineering in rice using prime editing system. Plant Biotechnology Journal, 18(11), 2167.

Hunziker, J., Nishida, K., Kondo, A., Kishimoto, S., Ariizumi, T., et al. (2020). Multiple gene substitution by Target-AID base-editing technology in tomato. Scientific Reports, 10(1), 20471.

Illouz-Eliaz, N., Nissan, I., Nir, I., Ramon, U., Shohat, H., et al. (2020). Mutations in the tomato gibberellin receptors suppress xylem proliferation and reduce water loss under water-deficit conditions. Journal of Experimental Botany, 71(12), 3603-3612.

Ito, Y., Nishizawa-Yokoi, A., Endo, M., Mikami, M., & Toki, S. (2015). CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochemical and Biophysical Research Communications, 467(1), 76-82.

Jiang, Y. Y., Chai, Y. P., Lu, M. H., Han, X. L., Lin, Q., et al. (2020). Prime editing efficiently generates W542L and S621I double mutations in two ALS genes in maize. Genome Biology, 21, 1-10.

Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096), 816-821.

Kaul, T., Sony, S. K., Verma, R., Motelb, K. F. A., Prakash, A. T., Eswaran, M., Bharti, J., Nehra, M., & Kaul, R. (2020). Revisiting CRISPR/Cas-mediated crop improvement: Special focus on nutrition. Journal of Biosciences, 45, 137.

Khan, N., Ray, R. L., Sargani, G. R., Ihtisham, M., Khayyam, M., et al. (2021). Current progress and future prospects of agriculture technology: Gateway to sustainable agriculture. Sustainability, 13(9), 4883.

Kim, H., Kim, S. T., Ryu, J., Kang, B. C., Kim, J. S., et al. (2017). CRISPR/Cpf1-mediated DNA-free plant genome editing. Nature Communications, 8(1), 14406.

Kim, S., Kim, D., Cho, S. W., Kim, J., & Kim, J. S. (2014). Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Research, 24(6), 1012-1019.

Klap, C., Yeshayahou, E., Bolger, A. M., Arazi, T., Gupta, S. K., et al. (2017). Tomato facultative parthenocarpy results from Sl AGAMOUS‐LIKE 6 loss of function. Plant Biotechnology Journal, 15(5), 634-647.

Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A., & Liu, D. R. (2016). Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 533(7603), 420-424.

Koonin, E. V., Makarova, K. S., & Zhang, F. (2017). Diversity, classification and evolution of CRISPR-Cas systems. Current Opinion in Microbiology, 37, 67-78.

Koseoglou, E., Hanika, K., Mohd Nadzir, M. M., Kohlen, W., Van Der Wolf, J. M., et al. (2023). Inactivation of tomato WAT1 leads to reduced susceptibility to Clavibacter michiganensis through downregulation of bacterial virulence factors. Frontiers in Plant Science, 14, 1082094.

Kumar, M., Chandran, D., Tomar, M., Bhuyan, D. J., Grasso, S., et al. (2022). Valorization potential of tomato (Solanum lycopersicum L.) seed: nutraceutical quality, food properties, safety aspects, and application as a health-promoting ingredient in foods. Horticulturae, 8(3), 265.

Kwon, C. T., Heo, J., Lemmon, Z. H., Capua, Y., Hutton, S. F., et al. (2020). Rapid customization of Solanaceae fruit crops for urban agriculture. Nature Biotechnology, 38(2), 182-188.

Leibman-Markus, M., Gupta, R., Schuster, S., Avni, A., & Bar, M. (2023). Members of the Tomato NRC4 h-NLR family augment each other in promoting basal immunity. Plant Science, 330, 111632.

Li, H., Li, J., Chen, J., Yan, L., & Xia, L. (2020). Precise modifications of both exogenous and endogenous genes in rice by prime editing. Molecular Plant, 13(5), 671-674.

Li, J., Sun, Y., Du, J., Zhao, Y., & Xia, L. (2017). Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Molecular plant, 10(3), 526-529.

Li, Q., Feng, Q., Snouffer, A., Zhang, B., Rodríguez, G. R., et al. (2022a). Increasing fruit weight by editing a cis-regulatory element in tomato KLUH promoter using CRISPR/Cas9. Frontiers in Plant Science, 13, 879642.

Li, R., Liu, C., Zhao, R., Wang, L., Chen, L., et al. (2019). CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biology, 19, 1-13.

Li, R., Maioli, A., Yan, Z., Bai, Y., Valentino, D., et al. (2022b). CRISPR/Cas9-Based Knockout of the PMR4 Gene Reduces Susceptibility to Late Blight in Two Tomato Cultivars. International Journal of Molecular Sciences, 23(23), 14542.

Li, R., Zhang, L., Wang, L., Chen, L., Zhao, R., et al. (2018a). Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. Journal of Agricultural and Food Chemistry, 66(34), 9042-9051.

Li, X., Wang, X., Sun, W., Huang, S., Zhong, M., et al. (2022c). Enhancing prime editing efficiency by modified pegRNA with RNA G-quadruplexes. Journal of Molecular Cell Biology, 14(4), mjac022.

Li, X., Wang, Y., Chen, S., Tian, H., Fu, D., et al. (2018b). Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Frontiers in Plant Science, 9, 559.

Lin, Q., Jin, S., Zong, Y., Yu, H., Zhu, Z., et al. (2021). High-efficiency prime editing with optimized, paired pegRNAs in plants. Nature Biotechnology, 39(8), 923-927.

Lin, Q., Zong, Y., Xue, C., Wang, S., Jin, S., et al. (2020). Prime genome editing in rice and wheat. Nature Biotechnology, 38(5), 582-585.

Liu, D., Shen, Z., Zhuang, K., Qiu, Z., Deng, H., et al. (2022). Systematic annotation reveals CEP function in tomato root development and abiotic stress response. Cells, 11(19), 2935.

Liu, H., Meng, F., Miao, H., Chen, S., Yin, T., et al. (2018). Effects of postharvest methyl jasmonate treatment on main health-promoting components and volatile organic compounds in cherry tomato fruits. Food Chemistry, 263, 194-200.

Liu, J., Wang, S., Wang, H., Luo, B., Cai, Y., et al. (2021). Rapid generation of tomato male-sterile lines with a marker use for hybrid seed production by CRISPR/Cas9 system. Molecular Breeding, 41, 1-12.

Liu, L., Zhang, J., Xu, J., Li, Y., Guo, L., et al. (2020a). CRISPR/Cas9 targeted mutagenesis of SlLBD40, a lateral organ boundaries domain transcription factor, enhances drought tolerance in tomato. Plant Science, 301, 110683.

Liu, M., Liang, Z., Aranda, M. A., Hong, N., Liu, L., et al. (2020b). A cucumber green mottle mosaic virus vector for virus-induced gene silencing incucurbit plants. Plant Methods, 16, 1-13.

Lu, H. P., Liu, S. M., Xu, S. L., Chen, W. Y., Zhou, X., et al. (2017). CRISPR‐S: an active interference element for a rapid and inexpensive selection of genome‐edited, transgene‐free rice plants. Plant Biotechnology journal, 15(11), 1371.

Lu, H., Fan, Y., Yuan, Y., Niu, X., Zhao, B., et al. (2023). Tomato SlSTK is involved in glucose response and regulated by the ubiquitin ligase SlSINA4. Plant Science, 331, 111672.

Lu, Y., Tian, Y., Shen, R., Yao, Q., Zhong, D., et al. (2021). Precise genome modification in tomato using an improved prime editing system. Plant Biotechnology Journal, 19(3), 415.

Marzec, M., Brąszewska-Zalewska, A., & Hensel, G. (2020). Prime editing: a new way for genome editing. Trends in Cell Biology, 30(4), 257-259.

Mendez‐López, E., Donaire, L., Gosálvez, B., Díaz‐Vivancos, P., Sánchez‐Pina, M. A., et al. (2023). Tomato SlGSTU38 interacts with the PepMV coat protein and promotes viral infection. New Phytologist, 238(1), 332-348.

Menz, J., Modrzejewski, D., Hartung, F., Wilhelm, R., & Sprink, T. (2020). Genome edited crops touch the market: a view on the global development and regulatory environment. Frontiers in Plant Science, 11, 586027.

Milon, R. B., Hu, P., Zhang, X., Hu, X., & Ren, L. (2024). Recent advances in the biosynthesis and industrial biotechnology of Gamma-amino butyric acid. Bioresources and Bioprocessing, 11(1), 32.

Mishra, R., Rout, E., & Joshi, R. K. (2019). Identification of resistant sources against anthracnose disease caused by Colletotrichum truncatum and Colletotrichum gloeosporioides in Capsicum annuum L. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 89, 517-524.

Mishra, R., Zheng, W., Joshi, R. K., & Kaijun, Z. (2021). Genome editing strategies towards enhancement of rice disease resistance. Rice Science, 28(2), 133-145.

Moon, S. B., Kim, D. Y., Ko, J. H., & Kim, Y. S. (2019). Recent advances in the CRISPR genome editing tool set. Experimental & Molecular Medicine, 51(11), 1-11.

Nekrasov, V., Wang, C., Win, J., Lanz, C., Weigel, D., et al. (2017). Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Scientific Reports, 7(1), 482.

Nie, H., Shi, Y., Geng, X., & Xing, G. (2022). CRISRP/Cas9-mediated targeted mutagenesis of tomato polygalacturonase gene (SlPG) delays fruit softening. Frontiers in Plant Science, 13, 729128.

Nishida, K., Arazoe, T., Yachie, N., Banno, S., Kakimoto, M., et al. (2016). Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science, 353(6305), aaf8729.

Nonaka, S., Arai, C., Takayama, M., Matsukura, C., & Ezura, H. (2017). Efficient increase of ɣ-aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Scientific Reports, 7(1), 7057.

Ortigosa, A., Gimenez‐Ibanez, S., Leonhardt, N., & Solano, R. (2019). Design of a bacterial speck resistant tomato by CRISPR/Cas9‐mediated editing of Sl JAZ 2. Plant Biotechnology Journal, 17(3), 665-673.

Perk, E. A., Arruebarrena Di Palma, A., Colman, S., Mariani, O., Cerrudo, I., et al. (2023). CRISPR/Cas9-mediated phospholipase C 2 knockout tomato plants are more resistant to Botrytis cinerea. Planta, 257(6), 117.

Perroud, P. F., Guyon-Debast, A., Veillet, F., Kermarrec, M. P., Chauvin, L., et al. (2022). Prime Editing in the model plant Physcomitrium patens and its potential in the tetraploid potato. Plant Science, 316, 111162.

Pramanik, D., Shelake, R. M., Park, J., Kim, M. J., Hwang, I., et al. (2021). CRISPR/Cas9-mediated generation of pathogen-resistant tomato against tomato yellow leaf curl virus and powdery mildew. International Journal of Molecular Sciences, 22(4), 1878.

Qin, R., Li, J., Li, H., Zhang, Y., Liu, X., et al. (2019). Developing a highly efficient and wildly adaptive CRISPR‐SaCas9 toolset for plant genome editing. Plant Biotechnology Journal, 17(4), 706.

Rather, G. A., Ayzenshtat, D., Teper-Bamnolker, P., Kumar, M., Forotan, Z., et al. (2022). Advances in protoplast transfection promote efficient CRISPR/Cas9-mediated genome editing in tetraploid potato. Planta, 256(1), 14.

Ren, Q., Sretenovic, S., Liu, S., Tang, X., Huang, L., et al. (2021). PAM-less plant genome editing using a CRISPR–SpRY toolbox. Nature Plants, 7(1), 25-33.

Rodríguez-Leal, D., Lemmon, Z. H., Man, J., Bartlett, M. E., & Lippman, Z. B. (2017). Engineering quantitative trait variation for crop improvement by genome editing. Cell, 171(2), 470-480.

Roosjen, M., Paque, S., &Weijers, D. (2018). Auxin response factors: output control in auxin biology. Journal of Experimental Botany, 69(2), 179-188.

Ruiz‐Ramón, F., Rodríguez‐Sepúlveda, P., Bretó, P., Donaire, L., Hernando, Y., et al. (2023). The tomato calcium‐permeable channel 4.1 (SlOSCA4. 1) is a susceptibility factor for pepino mosaic virus. Plant Biotechnology Journal, 21(10), 2140-2154.

Santillán Martínez, M. I., Bracuto, V., Koseoglou, E., Appiano, M., Jacobsen, E., et al. (2020). CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew. BMC Plant Biology, 20, 1-13.

Scholefield, J., & Harrison, P. T. (2021). Prime editing–an update on the field. Gene Therapy, 28(7), 396-401.

Shen, W., Zhang, J., Geng, B., Qiu, M., Hu, M., et al. (2019). Establishment and application of a CRISPR–Cas12a assisted genome-editing system in Zymomonas mobilis. Microbial Cell Factories, 18, 1-11.

Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., et al. (2017). Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nature Biotechnology, 35(5), 441-443.

Shu, P., Li, Y., Xiang, L., Sheng, J., & Shen, L. (2023). SlNPR1 modulates chilling stress resistance in tomato plant by alleviating oxidative damage and affecting the synthesis of ferulic acid. Scientia Horticulturae, 307, 111486.

Shu, P., Li, Z., Min, D., Zhang, X., Ai, W., et al. (2020). CRISPR/Cas9-mediated SlMYC2 mutagenesis adverse to tomato plant growth and MeJA-induced fruit resistance to Botrytis cinerea. Journal of Agricultural and Food Chemistry, 68(20), 5529-5538.

Soyk, S., Müller, N. A., Park, S. J., Schmalenbach, I., Jiang, K., et al. (2017). Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nature genetics, 49(1), 162–168. https://doi.org/10.1038/ng.3733.

Swinnen, G., Mauxion, J. P., Baekelandt, A., De Clercq, R., Van Doorsselaere, J., et al. (2022). SlKIX8 and SlKIX9 are negative regulators of leaf and fruit growth in tomato. Plant Physiology, 188(1), 382-396.

Thomazella, D. P. D. T., Seong, K., Mackelprang, R., Dahlbeck, D., Geng, Y., et al. (2021). Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. Proceedings of the National Academy of Sciences, 118(27), e2026152118.

Tieman, D., Zhu, G., Resende Jr, M. F., Lin, T., Nguyen, C., et al. (2017). A chemical genetic roadmap to improved tomato flavor. Science, 355(6323), 391-394.

Toda, E., Koiso, N., Takebayashi, A., Ichikawa, M., Kiba, T., et al. (2019). An efficient DNA-and selectable-marker-free genome-editing system using zygotes in rice. Nature Plants, 5(4), 363-368.

Tomlinson, L., Yang, Y., Emenecker, R., Smoker, M., Taylor, J., et al. (2019). Using CRISPR/Cas9 genome editing in tomato to create a gibberellin‐responsive dominant dwarf DELLA allele. Plant Biotechnology Journal, 17(1), 132-140.

Tran, M. T., Doan, D. T. H., Kim, J., Song, Y. J., Sung, Y. W., et al. (2021). CRISPR/Cas9-based precise excision of SlHyPRP1 domain (s) to obtain salt stress-tolerant tomato. Plant Cell Reports, 40, 999-1011.

Tsanova, T., Stefanova, L., Topalova, L., Atanasov, A., &Pantchev, I. (2021). DNA-free gene editing in plants: a brief overview. Biotechnology & Biotechnological Equipment, 35(1), 131-138.

Ueta, R., Abe, C., Watanabe, T., Sugano, S. S., Ishihara, R., et al. (2017). Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Scientific Reports, 7(1), 507.

Veillet, F., Perrot, L., Chauvin, L., Kermarrec, M. P., Guyon-Debast, A., et al. (2019). Transgene-free genome editing in tomato and potato plants using agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. International Journal of Molecular Sciences, 20(2), 402.

Vu, T. V., Sivankalyani, V., Kim, E. J., Doan, D. T. H., Tran, M. T., et al. (2020). Highly efficient homology‐directed repair using CRISPR/Cpf1‐geminiviral replicon in tomato. Plant Biotechnology Journal, 18(10), 2133-2143.

Waltz, E., (2022). GABA-enriched tomato is first CRISPR-edited food to enter market. National Biotechnology, 40(1), 9-11.

Wan, L., Wang, Z., Tang, M., Hong, D., Sun, Y., et al. (2021). CRISPR-Cas9 gene editing for fruit and vegetable crops: strategies and prospects. Horticulturae, 7(7), 193.

Wang, D., Samsulrizal, N. H., Yan, C., Allcock, N. S., Craigon, J., et al. (2019). Characterization of CRISPR mutants targeting genes modulating pectin degradation in ripening tomato. Plant Physiology, 179(2), 544-557.

Wang, L., Chen, L., Li, R., Zhao, R., Yang, M., et al. (2017). Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. Journal of Agricultural and Food Chemistry, 65(39), 8674-8682.

Wang, R., Angenent, G. C., Seymour, G., & de Maagd, R. A. (2020). Revisiting the role of master regulators in tomato ripening. Trends in Plant Science, 25(3), 291-301.

Wang, R., Liu, K., Tang, B., Su, D., He, X., et al. (2023). The MADS‐box protein SlTAGL1 regulates a ripening‐associated SlDQD/SDH2 involved in flavonoid biosynthesis and resistance against Botrytis cinerea in post‐harvest tomato fruit. The Plant Journal, 115(6), 1746-1757.

Wang, T., Deng, Z., Zhang, X., Wang, H., Wang, Y., et al. (2018). Tomato DCL2b is required for the biosynthesis of 22-nt small RNAs, the resulting secondary siRNAs, and the host defense against ToMV. Horticulture Research, 5, 62. https://doi.org/10.1038/s41438-018-0073-7

Wang, Z., Hong, Y., Li, Y., Shi, H., Yao, J., et al. (2021). Natural variations in SlSOS1 contribute to the loss of salt tolerance during tomato domestication. Plant Biotechnology Journal, 19(1), 20.

Wei, J., & Li, Y. (2023). CRISPR-based gene editing technology and its application in microbial engineering. Engineering Microbiology, 3 (4), 100101. https://doi.org/10.1016/j.engmic.2023.100101.

Woo, J. W., Kim, J., Kwon, S. I., Corvalán, C., Cho, S. W., et al. (2015). DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology, 33(11), 1162-1164.

Xu, D., Liu, X., Guo, C., Lin, L., & Yin, R. (2023). The B-box transcription factor 4 regulates seedling photomorphogenesis and flowering in tomato. Scientia Horticulturae, 309, 111692.

Xu, J., Hua, K., & Lang, Z. (2019). Genome editing for horticultural crop improvement. Horticulture Research, 6, 113.

Xu, R., Li, J., Liu, X., Shan, T., Qin, R., & Wei, P. (2020a). Development of Plant Prime-Editing Systems for Precise Genome Editing. Plant communications, 1(3), 100043. https://doi.org/10.1016/j.xplc.2020.100043

Xu, X., Yuan, Y., Feng, B., & Deng, W. (2020b). CRISPR/Cas9-mediated gene-editing technology in fruit quality improvement. Food Quality and Safety, 4(4), 159-166

Yang, Q., Wan, X., Wang, J., Zhang, Y., Zhang, J., Wang, T., Yang, C., & Ye, Z. (2020). The loss of function of HEL, which encodes a cellulose synthase interactive protein, causes helical and vine-like growth of tomato. Horticulture research, 7(1), 180. https://doi.org/10.1038/s41438-020-00402-0.

Yang, T., Ali, M., Lin, L., Li, P., He, H., et al. (2023). Recoloring tomato fruit by CRISPR/Cas9-mediated multiplex gene editing. Horticulture research, 10(1), uhac214. https://doi.org/10.1093/ hr/uhac214.

Yin, Y., Qin, K., Song, X., Zhang, Q., Zhou, Y., et al. (2018). BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase-mediated reactive oxygen species signaling in tomato. Plant and Cell Physiology, 59(11), 2239-2254.

Yoon, Y. J., Venkatesh, J., Lee, J. H., Kim, J., Lee, H. E., et al. (2020). Genome editing of eIF4E1 in tomato confers resistance to pepper mottle virus. Frontiers in Plant Science, 11, 1098.

Yu, W., Wang, L., Zhao, R., Sheng, J., Zhang, S., Li, R., & Shen, L. (2019). Knockout of SlMAPK3 enhances tolerance to heat

stress involving ROS homeostasis in tomato plants. BMC Plant Biology, 19, 1-13.

Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., et al. (2015). Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163(3), 759-771.

Zhang, S., Shen, J., Li, D., & Cheng, Y. (2021a). Strategies in the delivery of Cas9 ribonucleoprotein for CRISPR/Cas9 genome editing. Theranostics, 11(2), 614.

Zhang, Y., Restall, J., Crisp, P., Godwin, I., & Liu, G. (2021b). Current status and prospects of plant genome editing in Australia. In Vitro Cellular & Developmental Biology-Plant, 57(4), 574-583.