Advancements and challenges in CRISPR/cas genome editing for
legume crops

Tatiana Faria Maia; Joaquin Felipe Roca Paixão; Marcia Soares Vidal; Krzysztof Szczyglowski; Jean Luiz Simões de Araújo

doi:10.4322/biori.00132023

Review Article

Advancements and challenges in CRISPR/cas genome editing for legume crops

Tatiana Faria Maia; Joaquin Felipe Roca Paixão; Marcia Soares Vidal; Krzysztof Szczyglowski; Jean Luiz Simões de Araújo

http://dx.doi.org/10.4322/biori.00132023 BIORI, vol.8, n1, e2024013, 2024

PDF

Downloads: 3

Abstract

Agricultural systems are facing significant pressure due to population growth, water scarcity, and the impacts of climate change, which collectively pose a threat to global food security. In this scenario, leguminous plants play a crucial role as they are an excellent source of protein for human nutrition. Additionally, they can symbiotically fix nitrogen with soil bacteria, thereby reducing soil contamination and emissions of nitrous oxide and ammonia. However, the yield of legumes is threatened by biotic stresses, such as diseases and pests, as well as abiotic environmental factors, which ultimately affect nutritional quality and productivity. Advancements in genetic engineering offer new approaches for improving crops. The CRISPR/ Cas system, an innovative biotechnology tool, allows for precise and efficient modifications of the genome, enabling the creation of new traits in legume plants. In this review, we explore the relevant applications, challenges, and potential of the CRISPR/Cas system in enhancing the yield and adaptability of leguminous crops.

Supplementary Material

Keywords

Leguminous plants; Gene editing; CRISPR/Cas9; Crop breeding

References

Adachi, K., Hirose, A., Kanazashi, Y., Hibara, M., Hirata, T., Mikami, M., Endo, M., Hirose, S., Maruyama, N., Ishimoto, M., Abe, J., & Yamada, T. (2021). Site-directed mutagenesis by biolistic transformation efficiently generates inheritable mutations in a targeted locus in soybean somatic embryos and transgene-free descendants in the T 1 generation. Transgenic Research, 30(1), 77- 89. http://doi.org/10.1007/s11248-020-00229-4. PMid:33386504.

Al Amin, N., Ahmad, N., Wu, N., Pu, X., Ma, T., Du, Y., Bo, X., Wang, N., Sharif, R., & Wang, P. (2019). CRISPR-Cas9 mediated targeted disruption of FAD2–2 microsomal omega-6 desaturase in soybean (Glycine max. L). BMC Biotechnology, 19(1), 9. http:// doi.org/10.1186/s12896-019-0501-2. PMid:30691438.

Alamillo, J. M., López, C. M., Rivas, F. J. M., Torralbo, F., Bulut, M., & Alseekh, S. (2023). Clustered regularly interspaced short palindromic repeats/CRISPR-associated protein and hairy roots: A perfect match for gene functional analysis and crop improvement. Current Opinion in Biotechnology, 79, 102876. http://doi. org/10.1016/j.copbio.2022.102876. PMid:36621223.

Alok, A., Jain, P., Kumar, J., Yajnik, K., & Bhalothia, P. (2020). Genome engineering in medicinally important plants using CRISPR/Cas9 tool. In V. Singh, & P. K. Dhar (Eds.), Genome engineering via CRISPR-Cas9 system (pp. 155-161). Academic Press. http://doi. org/10.1016/B978-0-12-818140-9.00014-3.

Altpeter, F., Baisakh, N., Beachy, R., Bock, R., Capell, T., Christou, P., Daniell, H., Datta, K., Datta, S., Dix, P. J., Fauquet, C., Huang, N., Kohli, A., Mooibroek, H., Nicholson, L., Nguyen, T. T., Nugent, G., Raemakers, K., Romano, A., Somers, D. A., Stoger, E., Taylor, N., & Visser, R. (2005). Particle bombardment and the genetic enhancement of crops: Myths and realities. Molecular Breeding, 15(3), 305-327. http://doi.org/10.1007/s11032-004-8001-y.

Altpeter, F., Springer, N. M., Bartley, L. E., Blechl, A. E., Brutnell, T. P., Citovsky, V., Conrad, L. J., Gelvin, S. B., Jackson, D. P., Kausch, A. P., Lemaux, P. G., Medford, J. I., Orozco-Cárdenas, M. L., Tricoli, D. M., Van Eck, J., Voytas, D. F., Walbot, V., Wang, K., Zhang, Z. J., & Stewart Junior, C. N. (2016). Advancing crop transformation in the era of genome editing. The Plant Cell, 28(7), 1510-1520. http://doi.org/10.1105/tpc.16.00196. PMid:27335450.

Aman, R., Ali, Z., Butt, H., Mahas, A., Aljedaani, F., & Khan, M. Z. (2018). RNA virus interference via CRISPR/Cas13a system in plants. Genome Biology, 1-9. https://doi.org/10.1186/s13059- 017-1381-1.

Andersson, M., Turesson, H., Olsson, N., Fält, A. S., Ohlsson, P., Gonzalez, M. N., Samuelsson, M., & Hofvander, P. (2018). Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiologia Plantarum, 164(4), 378-384. http://doi.org/10.1111/ ppl.12731. PMid:29572864.

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. http://doi. org/10.1038/s41587-020-0561-9. PMid:32572269.

Anzalone, A. V., Randolph, P. B., Davis, J. R., Sousa, A. A., Koblan, L. W., Levy, J. M., Chen, P. J., Wilson, C., Newby, G. A., Raguram, A., & Liu, D. R. (2019). Search-and-replace genome editing without double-strand breaks or donor DNA. Nature, 576(7785), 149-157. http://doi.org/10.1038/s41586-019-1711-4. PMid:31634902.

Arabidopsis Genome Initiative. (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408(6814), 796-815. http://doi.org/10.1038/35048692. PMid:11130711.

Arnoldi, A., Boschin, G., Zanoni, C., & Lammi, C. (2015). The health benefits of sweet lupin seed flours and isolated proteins. Journal of Functional Foods, 18, 550-563. http://doi.org/10.1016/j. jff.2015.08.012.

Babar, M. M., Zaidi, N. U. S. S., Azooz, M. M., & Kazi, A. G. Genetic and molecular responses of legumes in a changing environment. (2015). Legumes under environmental stress: yield, improvement and adaptations, 199-214. https://doi. org/10.1002/9781118917091.ch12

Badhan, S., Ball, A. S., & Mantri, N. (2021). First report of CRISPR/ Cas9 mediated DNA-free editing of 4CL and RVE7 genes in chickpea protoplasts. International Journal of Molecular Sciences, 22(1), 396. https://doi.org/10.3390/ijms22010396.

Bahramnejad, B., Naji, M., Bose, R., & Jha, S. (2019). A critical review on use of Agrobacterium rhizogenes and their associated binary vectors for plant transformation. Biotechnology Advances, 37(7), 107405. http://doi.org/10.1016/j.biotechadv.2019.06.004. PMid:31185263.

Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E., & Schroeder, J. I. (2019). Genetic strategies for improving crop yields. Nature, 575(7781), 109-118. http://doi.org/10.1038/ s41586-019-1679-0. PMid:31695205.

Baltes, N. J., Gil-Humanes, J., & Voytas, D. F. (2017). Genome engineering and agriculture: Opportunities and challenges. Progress in Molecular Biology and Translational Science, 149, 1-26. http://doi.org/10.1016/bs.pmbts.2017.03.011. PMid:28712492.

Banakar, R., Eggenberger, A. L., Lee, K., Wright, D. A., Murugan, K., Zarecor, S., Lawrence-Dill, C. J., Sashital, D. G., & Wang, K. (2019). High-frequency random DNA insertions upon co-delivery of CRISPR-Cas9 ribonucleoprotein and selectable marker plasmid in rice. Scientific Reports, 9(1), 19902. http://doi.org/10.1038/ s41598-019-55681-y. PMid:31882637.

Banakar, R., Schubert, M., Kurgan, G., Rai, K. M., Beaudoin, S. F., Collingwood, M. A., Vakulskas, C. A., Wang, K., & Zhang, F. (2022). Efficiency, specificity and temperature sensitivity of Cas9 and Cas12a RNPs for DNA-free genome editing in plants. Frontiers in Genome Editing, 3, 41. http://doi.org/10.3389/ fgeed.2021.760820. PMid:35098208.

Bao, A., Chen, H., Chen, L., Chen, S., Hao, Q., Guo, W., Qiu, D., Shan, Z., Yang, Z., Yuan, S., Zhang, C., Zhang, X., Liu, B., Kong, F., Li, X., Zhou, X., Tran, L. P., & Cao, D. (2019). CRISPR/Cas9- mediated targeted mutagenesis of GmSPL9 genes alters plant architecture in soybean. BMC Plant Biology, 19(1), 1-12. http:// doi.org/10.1186/s12870-019-1746-6. PMid:30961525.

Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., & Horvath, P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315(5819), 1709-1712. http://doi.org/10.1126/science.1138140. PMid:17379808.

Bertioli, D. J., Jenkins, J., Clevenger, J., Dudchenko, O., Gao, D., Seijo, G., Leal-Bertioli, S. C. M., Ren, L., Farmer, A. D., Pandey, M. K., Samoluk, S. S., Abernathy, B., Agarwal, G., Ballén-Taborda, C., Cameron, C., Campbell, J., Chavarro, C., Chitikineni, A., Chu, Y., Dash, S., El Baidouri, M., Guo, B., Huang, W., Kim, K. D., Korani, W., Lanciano, S., Lui, C. G., Mirouze, M., Moretzsohn, M. C., Pham, M., Shin, J. H., Shirasawa, K., Sinharoy, S., Sreedasyam, A., Weeks, N. T., Zhang, X., Zheng, Z., Sun, Z., Froenicke, L., Aiden, E. L., Michelmore, R., Varshney, R. K., Holbrook, C. C., Cannon, E. K. S., Scheffler, B. E., Grimwood, J., Ozias-Akins, P., Cannon, S. B., Jackson S. A., & Schmutz J. (2019). The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nature Genetics, 51(5), 877-884. http://doi.org/10.1038/s41588- 019-0405-z. PMid:31043755.

Bhajan, S. K., Begum, S., Islam, M. N., Hoque, M. I., & Sarker, R. H. (2019). In vitro regeneration and Agrobacterium-mediated genetic transformation of local varieties of mungbean (Vigna radiata (L). Wilczek). Plant Tissue Culture & Biotechnology, 29(1), 81-97. http://doi.org/10.3329/ptcb.v29i1.41981.

Bhowmik, P., Konkin, D., Polowick, P., Hodgins, C. L., Subedi, M., Xiang, D., Yu, B., Patterson, N., Rajagopalan, N., Babic, V., Ro, D.-K., Tar’an, B., Bandara, M., Smyth, S. J., Cui, Y., & Kagale, S. (2021). CRISPR/Cas9 gene editing in legume crops: Opportunities and challenges. Legume Science, 3(3), e96. https:// doi.org/10.1002/leg3.96.

Biswas, S., Bridgeland, A., Irum, S., Thomson, M. J., & Septiningsih, E. M. (2022). Optimization of prime editing in rice, peanut, chickpea, and cowpea protoplasts by restoration of GFP activity. International Journal of Molecular Sciences, 23(17), 9809. http:// doi.org/10.3390/ijms23179809. PMid:36077206.

Bolotin, A., Quinquis, B., Sorokin, A., & Ehrlich, S. D. (2005). Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 151(8), 2551- 2561. http://doi.org/10.1099/mic.0.28048-0. PMid:16079334.

Borrelli, V. M., Brambilla, V., Rogowsky, P., Marocco, A., & Lanubile, A. (2018). The enhancement of plant disease resistance using CRISPR/Cas9 technology. Frontiers in Plant Science, 9, 1245. http://doi.org/10.3389/fpls.2018.01245. PMid:30197654.

Bortesi, L., & Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnology Advances, 33(1), 41-52. http://doi.org/10.1016/j.biotechadv.2014.12.006. PMid:25536441.

Bottero, E., Gómez, C., Stritzler, M., Tajima, H., Frare, R., Pascuan, C., Blumwald, E., Ayub, N., & Soto, G. (2022). Generation of a multi-herbicide-tolerant alfalfa by using base editing. Plant Cell Reports, 41(2), 493-495. http://doi.org/10.1007/s00299-021- 02827-w. PMid:34994854.

Brasil. Comissão Técnica Nacional de Biossegurança. (2018). Estabelece os requisitos técnicos para apresentação de consulta à CTNBio sobre as Técnicas Inovadoras de Melhoramento de Precisão (Resolução Normativa Nº 16, de 15 de janeiro de 2018).

Brouns, S. J. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J. H., Snijders, A. P. L., Dickman, M. J., Makarova, K. S., Koonin, E. V., & Van Der Oost, J. (2008). Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321(5891), 960-964. http://doi. org/10.1126/science.1159689. PMid:18703739.

Cabanillas, B., Jappe, U., & Novak, N. (2018). Allergy to peanut, soybean, and other legumes: Recent advances in allergen characterization, stability to processing and IgE cross-reactivity. Molecular Nutrition & Food Research, 62(1), 1700446. http:// doi.org/10.1002/mnfr.201700446. PMid:28944625.

Cai, Y., Chen, L., Liu, X., Sun, S., Wu, C., Jiang, B., Han, T., & Hou, W. (2015). CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS One, 10(8), 0136064. https://doi.org/10.1371/ journal.pone.0136064.

Cai, Y., Chen, L., Liu, X., Guo, C., Sun, S., Wu, C., Jiang, B., Han, T., & Hou, W. (2018a). CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnology Journal, 16(1), 176-185. http://doi.org/10.1111/ pbi.12758. PMid:28509421.

Cai, Y., Chen, L., Sun, S., Wu, C., Yao, W., Jiang, B., Han, T., & Hou, W. (2018b). CRISPR/Cas9-mediated deletion of large genomic fragments in soybean. International Journal of Molecular Sciences, 19(12), 3835. http://doi.org/10.3390/ijms19123835. PMid:30513774.

Cai, Y., Wang, L., Chen, L., Wu, T., Liu, L., Sun, S., Wu, C., Yao, W., Jiang, B., Yuan, S., Han, T., & Hou, W. (2020a). Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean. Plant Biotechnology Journal, 18(1), 298-309. http://doi.org/10.1111/ pbi.13199. PMid:31240772.

Cai, Y., Chen, L., Zhang, Y., Yuan, S., Su, Q., Sun, S., Wu, C., Yao, W., Han, T., & Hou, W. (2020b). Target base editing in soybean using a modified CRISPR/Cas9 system. Plant Biotechnology Journal, 18(10), 1996-1998. http://doi.org/10.1111/pbi.13386. PMid:32311214.

Çakir, Ö., Uçarli, C., Tarhan, Ç., Pekmez, M., & Turgut-Kara, N. (2019). Nutritional and health benefits of legumes and their distinctive genomic properties. Food Science and Technology (Campinas), 39(1), 1-12. http://doi.org/10.1590/fst.42117.

Calzadilla, P. I., Vilas, J. M., Escaray, F. J., Unrein, F., Carrasco, P., & Ruiz, O. A. (2019). The increase of photosynthetic carbon assimilation as a mechanism of adaptation to low temperature in Lotus japonicus, 1–15. https://doi.org/10.1038/s41598-018- 37165-7.

Campbell, B. W., Hoyle, J. W., Bucciarelli, B., Stec, A. O., Samac, D. A., Parrott, W. A., & Stupar, R. M. (2019). Functional analysis and development of a CRISPR/Cas9 allelic series for a CPR5 ortholog necessary for proper growth of soybean trichomes. Scientific Reports, 9(1), 1-11. http://doi.org/10.1038/s41598-019-51240- 7. PMid:31611562.

Čermák, T., Curtin, S. J., Gil-Humanes, J., Čegan, R., Kono, T. J., Konečná, E., Belanto, J. J., Starker, C. G., Mathre, J. W., Greenstein, R. L., & Voytas, D. F. (2017). A multipurpose toolkit to enable advanced genome engineering in plants. The Plant Cell, 29(6), 1196-1217. http://doi.org/10.1105/tpc.16.00922. PMid:28522548.

Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A., Arazi, T., & Gal-On, A. (2016). Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Molecular Plant Pathology, 17(7), 1140-1153. http://doi.org/10.1111/mpp.12375. PMid:26808139.

Che, P., Chang, S., Simon, M. K., Zhang, Z., Shaharyar, A., Ourada, J., O’Neill, D., Torres-Mendoza, M., Guo, Y., Marasigan, K. M., Vielle-Calzada, J.-P., Ozias-Akins, P., Albertsen, M. C., & Jones, T. J. (2021). Developing a rapid and highly efficient cowpea regeneration, transformation and genome editing system using embryonic axis explants. The Plant Journal, 106(3), 817-830. http://doi.org/10.1111/tpj.15202. PMid:33595147.

Chen, L., Cai, Y., Liu, X., Yao, W., Guo, C., Sun, S., Wu, C., Jiang, B., Han, T., & Hou, W. (2018). Improvement of soybean Agrobacteriummediated transformation efficiency by adding glutamine and asparagine into the culture media. International Journal of Molecular Sciences, 19(10), 3039. http://doi.org/10.3390/ ijms19103039. PMid:30301169.

Chen, R. (2018). Functional genomics and genetic control of compound leaf development in Medicago truncatula: An overview. Functional Genomics in Medicago truncatula. Methods and Protocols, 1822, 197-203. http://doi.org/10.1007/978-1-4939-8633-0_14. PMid:30043306.

Cheng, N., & Nakata, P. A. (2020). Development of a rapid and efficient protoplast isolation and transfection method for chickpea (Cicer arietinum). MethodsX, 7, 101025. http://doi.org/10.1016/j. mex.2020.101025. PMid:32874941.

Cheng, Q., Dong, L., Su, T., Li, T., Gan, Z., Nan, H., Lu, S., Fang, C., Kong, L., Li, H., Hou, Z., Kou, K., Tang, Y., Lin, X., Zhao, X., Chen, L., Liu, B., & Kong, F. (2019). CRISPR/Cas9-mediated targeted mutagenesis of GmLHY genes alters plant height and internode length in soybean. BMC Plant Biology, 19(1), 1-11. http://doi.org/10.1186/s12870-019-2145-8. PMid:31852439.

Cho, H. J., Moy, Y., Rudnick, N. A., Klein, T. M., Yin, J., Bolar, J., Hendrick, C., Beatty, M., Castañeda, L., Kinney, A. J., Jones, T. J., & Chilcoat, N. D. (2022). Development of an efficient marker-free soybean transformation method using the novel bacterium Ochrobactrum haywardense H1. Plant Biotechnology Journal, 20(5), 977-990. http://doi.org/10.1111/pbi.13777. PMid:35015927.

Cho, S. W., Kim, S., Kim, J. M., & Kim, J. S. (2013). Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nature Biotechnology, 31(3), 230-232. http:// doi.org/10.1038/nbt.2507. PMid:23360966.

Choudhury, A., & Rajam, M. V. (2021). Genetic transformation of legumes: An update. Plant Cell Reports, 40(10), 1813-1830. http://doi.org/10.1007/s00299-021-02749-7. PMid:34230986.

Chu, P., & Agapito-Tenfen, S. Z. (2022). Unintended Genomic Outcomes in Current and Next Generation GM Techniques: A Systematic Review. Plants, 11(21), 2997. http://doi.org/10.3390/ plants11212997. PMid:36365450.

Confalonieri, M., Carelli, M., Gianoglio, S., Moglia, A., Biazzi, E., & Tava, A. (2021). CRISPR/Cas9-mediated targeted mutagenesis of CYP93E2 modulates the triterpene saponin biosynthesis in Medicago truncatula. Frontiers in Plant Science, 12, 690231. http://doi.org/10.3389/fpls.2021.690231. PMid:34381478.

Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., & Zhang, F. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science, 339(6121), 819-823. http://doi.org/10.1126/science.1231143. PMid:23287718.

Court of Justice of the European Union. (2018). Organisms obtained by mutagenesis are GMOs and are, in principle, subject to the obligations laid down by the GMO directive. Press Release. Curtin, S. J., Xiong, Y., Michno, J. M., Campbell, B. W., Stec, A. O., Čermák, T., Starker, C., Voytas, D. F., Eamens, A. L., & Stupar, R. M. (2018). Crispr/cas9 and talen s generate heritable mutations for genes involved in small rna processing of glycine max and medicago truncatula. Plant Biotechnology Journal, 16(6), 1125- 1137. http://doi.org/10.1111/pbi.12857. PMid:29087011.

Deltcheva, E., Chylinski, K., Sharma, C. M., Gonzales, K., Chao, Y., Pirzada, Z. A., Eckert, M. R., Vogel, J., & Charpentier, E. (2011). CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471(7340), 602-607. http://doi. org/10.1038/nature09886. PMid:21455174.

Délye, C., Jasieniuk, M., & Le Corre, V. (2013). Deciphering the evolution of herbicide resistance in weeds. Trends in Genetics, 29(11), 649-658. http://doi.org/10.1016/j.tig.2013.06.001. PMid:23830583.

Deveau, H., Barrangou, R., Garneau, J. E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D. A., Horvath, P., & Moineau, S. (2008). Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. Journal of Bacteriology, 190(4), 1390-1400. http:// doi.org/10.1128/JB.01412-07. PMid:18065545.

Do, P. T., Nguyen, C. X., Bui, H. T., Tran, L. T., Stacey, G., Gillman, J. D., Zhang, Z. J., & Stacey, M. G. (2019). Demonstration of highly efficient dual gRNA CRISPR/Cas9 editing of the homeologous GmFAD2–1A and GmFAD2–1B genes to yield a high oleic, low linoleic and α-linolenic acid phenotype in soybean. BMC Plant Biology, 19(1), 311. http://doi.org/10.1186/s12870-019-1906-8. PMid:31307375.

Dolgikh, A. V., Kirienko, A. N., Tikhonovich, I. A., Foo, E., & Dolgikh, E. A. (2019). The DELLA proteins influence the expression of cytokinin biosynthesis and response genes during nodulation. Frontiers in Plant Science, 10, 432. http://doi.org/10.3389/ fpls.2019.00432. PMid:31024597.

Doudna, J. A., & Charpentier, E. (2014). The new frontier of genome engineering with CRISPR-Cas9. Science, 346(6213), 1258096. http://doi.org/10.1126/science.1258096. PMid:25430774.

Du, Y. T., Zhao, M. J., Wang, C. T., Gao, Y., Wang, Y. X., Liu, Y. W., Chen, M., Chen, J., Zhou, Y. B., & Ma, Y. Z. (2018). Identification and characterization of GmMYB118 responses to drought and salt stress. BMC Plant Biology, 18, 320. http://doi.org/10.1186/ s12870-018-1551-7. PMid:30509166. Duan, K., Cheng, Y., Ji, J., Wang, C., Wei, Y., & Wang, Y. (2021). Large chromosomal segment deletions by CRISPR/LbCpf1-mediated multiplex gene editing in soybean. Journal of Integrative Plant Biology, 63(9), 1620-1631. http://doi.org/10.1111/jipb.13158. PMid:34331750.

Eckerstorfer, M. F., Engelhard, M., Heissenberger, A., Simon, S., & Teichmann, H. (2019). Plants developed by new genetic modification techniques: Comparison of existing regulatory frameworks in the EU and non-EU countries. Frontiers in Bioengineering and Biotechnology, 7, 26. http://doi.org/10.3389/ fbioe.2019.00026. PMid:30838207.

Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., & Kiss, G. B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature, 417(6892), 962-966. http://doi. org/10.1038/nature00842. PMid:12087406.

FAO - United Nations Food and Agriculture Organization. (2016). Year of pulse crops. http://www.fao.org/pulses-2016/en/.

Fritsche, S., Poovaiah, C., MacRae, E., & Thorlby, G. (2018). A New Zealand perspective on the application and regulation of gene editing. Frontiers in Plant Science, 9, 1323. http://doi. org/10.3389/fpls.2018.01323. PMid:30258454.

Gao, R., Feyissa, B. A., Croft, M., & Hannoufa, A. (2018). Gene editing by CRISPR / Cas9 in the obligatory outcrossing Medicago sativa. Planta, 247(4), 1043-1050. http://doi.org/10.1007/ s00425-018-2866-1. PMid:29492697.

Garneau, J. E., Dupuis, M. È., Villion, M., Romero, D. A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A. H., & Moineau, S. (2010). The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468(7320), 67-71. http://doi.org/10.1038/nature09523. PMid:21048762.

Gelvin, S. B. (2012). Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Frontiers in Plant Science, 3, 52. http://doi.org/10.3389/fpls.2012.00052. PMid:22645590.

Ghogare, R., Ludwig, Y., Bueno, G. M., Slamet-Loedin, I. H., & Dhingra, A. (2021). Genome editing reagent delivery in plants. Transgenic Research, 30(4), 321-335. http://doi.org/10.1007/ s11248-021-00239-w. PMid:33728594.

Guo, B., Sun, L., Jiang, S., Ren, H., Sun, R., Wei, Z., Wei, Z., Hong, H., Luan, X., Wang, J., Wang, X., Xu, D., Li, W., Guo, C., & Qiu, L.-J. (2022). Soybean genetic resources contributing to sustainable protein production. Theoretical and Applied Genetics, 135(11), 4095-4121. http://doi.org/10.1007/s00122-022-04222- 9. PMid:36239765.

Gupta, R. M., & Musunuru, K. (2014). Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9. The Journal of Clinical Investigation, 124(10), 4154-4161. http://doi.org/10.1172/ JCI72992. PMid:25271723. Gupta, S., Kumar, A., Patel, R., & Kumar, V. (2021). Genetically modified crop regulations: Scope and opportunity using the CRISPR-Cas9 genome editing approach. Molecular Biology Reports, 48(5), 4851-4863. http://doi.org/10.1007/s11033-021-06477-9. PMid:34114124.

Hada, A., Krishnan, V., Jaabir, M., Kumari, A., Jolly, M., Praveen, S., & Sachdev, A. (2018). Improved Agrobacterium tumefaciensmediated transformation of soybean [Glycine max (L.) Merr.] following optimization of culture conditions and mechanical techniques. In Vitro Cellular & Developmental Biology. Plant, 54(6), 672-688. http://doi.org/10.1007/s11627-018-9944-8.

Haque, E., Taniguchi, H., Hassan, M. M., Bhowmik, P., Karim, M. R., Śmiech, M., Zhao, K., Rahman, M., & Islam, T. (2018). Application of CRISPR/Cas9 genome editing technology for the improvement of crops cultivated in tropical climates: Recent progress, prospects, and challenges. Frontiers in Plant Science, 9, 617. http://doi. org/10.3389/fpls.2018.00617. PMid:29868073.

Hastwell, A. H., Gresshoff, P. M., & Ferguson, B. J. (2015). Genomewide annotation and characterization of CLAVATA/ESR (CLE) peptide hormones of soybean (Glycine max) and common bean (Phaseolus vulgaris), and their orthologues of Arabidopsis thaliana. Journal of Experimental Botany, 66(17), 5271-5287. http://doi. org/10.1093/jxb/erv351. PMid:26188205.

Haun, W., Coffman, A., Clasen, B. M., Demorest, Z. L., Lowy, A., Ray, E., Retterath, A., Stoddard, T., Juillerat, A., Cedrone, F., Mathis, L., Voytas, D. F., & Zhang, F. (2014). Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 genes family. Plant Biotechnology Journal, 12(7), 934-940. http://doi.org/10.1111/pbi.12201. PMid:24851712.

Hedden, P., & Sponsel, V. (2015). A Century of Gibberellin Research. Journal of Plant Growth Regulation, 34(4), 740-760. http://doi. org/10.1007/s00344-015-9546-1. PMid:26523085.

Horvath, P., Coûté-Monvoisin, A. C., Romero, D. A., Boyaval, P., Fremaux, C., & Barrangou, R. (2009). Comparative analysis of CRISPR loci in lactic acid bacteria genomes. International Journal of Food Microbiology, 131(1), 62-70. http://doi.org/10.1016/j. ijfoodmicro.2008.05.030. PMid:18635282.

Hou, S., Liu, Z., Shen, H., & Wu, D. (2019). Damage-associated molecular pattern-triggered immunity in plants. Frontiers in Plant Science, 10, 646. http://doi.org/10.3389/fpls.2019.00646. PMid:31191574.

Huang, P., Lu, M., Li, X., Sun, H., Cheng, Z., Miao, Y., Fu, Y., & Zhang, X. (2022). An Efficient Agrobacterium rhizogenes-Mediated Hairy Root Transformation Method in a Soybean Root Biology Study. International Journal of Molecular Sciences, 23(20), 12261. http://doi.org/10.3390/ijms232012261. PMid:36293115.

Hwang, H. H., Yu, M., & Lai, E. M. (2017). Agrobacterium-mediated plant transformation: Biology and applications. The Arabidopsis Book / American Society of Plant Biologists, 15, e0186. http:// doi.org/10.1199/tab.0186. PMid:31068763.

Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J.-R. J., & Joung, J. K. (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnology, 31(3), 227-229. http://doi.org/10.1038/nbt.2501. PMid:23360964.

Ishino, Y., Krupovic, M., & Forterre, P. (2018). History of CRISPR-Cas from encounter with a mysterious repeated sequence to genome editing technology. Journal of Bacteriology, 200(7), e00580-e17. http://doi.org/10.1128/JB.00580-17. PMid:29358495.

Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., & Nakata, A. (1987). Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Journal of Bacteriology, 169(12), 5429-5433. http://doi.org/10.1128/jb.169.12.5429- 5433.1987. PMid:3316184.

Ishizaki, K., Chiyoda, S., Yamato, K. T., & Kohchi, T. (2008). Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant & Cell Physiology, 49(7), 1084-1091. http://doi.org/10.1093/ pcp/pcn085. PMid:18535011.

Jacobs, T. B., LaFayette, P. R., Schmitz, R. J., & Parrott, W. A. (2015). Targeted genome modifications in soybean with CRISPR/ Cas9. BMC Biotechnology, 15, 16. http://doi.org/10.1186/s12896- 015-0131-2. PMid:25879861.

Jacobs, T. B., Zhang, N., Patel, D., & Martin, G. B. (2017). Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiology, 174(4), 2023-2037. http://doi. org/10.1104/pp.17.00489. PMid:28646085.

Jansen, R., Embden, J. D. V., Gaastra, W., & Schouls, L. M. (2002). Identification of genes that are associated with DNA repeats in prokaryotes. Molecular Microbiology, 43(6), 1565-1575. http:// doi.org/10.1046/j.1365-2958.2002.02839.x. PMid:11952905.

Jansing, J., Schiermeyer, A., Schillberg, S., Fischer, R., & Bortesi, L. (2019). Genome editing in agriculture: Technical and practical considerations. International Journal of Molecular Sciences, 20(12), 2888. http://doi.org/10.3390/ijms20122888. PMid:31200517.

Jenkins, J. A., Griffiths-Jones, S., Shewry, P. R., Breiteneder, H., & Mills, E. C. (2005). Structural relatedness of plant food allergens with specific reference to cross-reactive allergens: An in silico analysis. The Journal of Allergy and Clinical Immunology, 115(1), 163-170. http://doi.org/10.1016/j.jaci.2004.10.026. PMid:15637564.

Ji, J., Zhang, C., Sun, Z., Wang, L., Duanmu, D., & Fan, Q. (2019). Genome editing in cowpea Vigna unguiculata using CRISPR-Cas9. International Journal of Molecular Sciences, 20(10), 2471. http:// doi.org/10.3390/ijms20102471. PMid:31109137.

Jia, N., Zhu, Y., & Xie, F. (2018). An efficient protocol for model legume root protoplast isolation and transformation. Frontiers in Plant Science, 9, 670. http://doi.org/10.3389/fpls.2018.00670. PMid:29915605.

Jiao, K., Li, X., Su, S., Guo, W., Guo, Y., Guan, Y., Hu, Z., Shen, Z., & Luo, D. (2019). Genetic control of compound leaf development in the mungbean (Vigna radiata L.). Horticulture Research, 6(1), 23. http://doi.org/10.1038/s41438-018-0088-0. PMid:30729013.

Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., Zhang, X., Dai, H., Yang, J., & Wang, E. (2016). DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications, 7(1), 1-14. http://doi. org/10.1038/ncomms12433. PMid:27514472.

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. http://doi.org/10.1126/science.1225829. PMid:22745249.

Jinek, M., East, A., Cheng, A., Lin, S., Ma, E., & Doudna, J. (2013). RNA-programmed genome editing in human cells. elife, 2, e00471. http://dx.doi.org/10.7554/eLife.00471.

Jung, C., & Müller, A. E. (2009). Flowering time control and applications in plant breeding. Trends in Plant Science, 14(10), 563-573. http://doi.org/10.1016/j.tplants.2009.07.005. PMid:19716745.

Juranić, M., Nagahatenna, D. S., Salinas-Gamboa, R., Hand, M. L., Sánchez-León, N., Leong, W. H., How, T., Bazanova, N., Spriggs, A., Vielle-Calzada, J.-P., & Koltunow, A. M. G. (2020). A detached leaf assay for testing transient gene expression and gene editing in cowpea (Vigna unguiculata [L.] Walp.). Plant Methods, 16(1), 1-17. http://doi.org/10.1186/s13007-020-00630-4. PMid:32549904.

Kantor, A., McClements, M. E., & MacLaren, R. E. (2020). CRISPRCas9 DNA base-editing and prime-editing. International Journal of Molecular Sciences, 21(17), 6240. http://doi.org/10.3390/ ijms21176240. PMid:32872311.

Karthik, S., Pavan, G., & Manickavasagam, M. (2020). Nitric oxide donor regulates Agrobacterium-mediated genetic transformation efficiency in soybean [Glycine max (L.) Merrill]. Plant Cell, Tissue and Organ Culture, 141(3), 655-660. http://doi.org/10.1007/ s11240-020-01808-3.

Kim, H., & Choi, J. (2021). A robust and practical CRISPR/crRNA screening system for soybean cultivar editing using LbCpf1 ribonucleoproteins. Plant Cell Reports, 40(6), 1059-1070. http:// doi.org/10.1007/s00299-020-02597-x. PMid:32945949.

Kim, J. S. (2018). Precision genome engineering through adenine and cytosine base editing. Nature Plants, 4(3), 148-151. http:// doi.org/10.1038/s41477-018-0115-z. PMid:29483683.

Kim, H., Kim, S. T., Ryu, J., Kang, B. C., Kim, J. S., & Kim, S. G. (2017a). CRISPR/Cpf1-mediated DNA-free plant genome editing. Nature Communications, 8, 14406. http://doi.org/10.1038/ ncomms14406. PMid:28205546.

Kim, S. K., Seong, W., Han, G. H., Lee, D. H., & Lee, S. G. (2017b). CRISPR interference-guided multiplex repression of endogenous competing pathway genes for redirecting metabolic flux in Escherichia coli. Microbial Cell Factories, 16(1), 188. http:// doi.org/10.1186/s12934-017-0802-x. PMid:29100516.

Kloosterman, B., Anithakumari, A. M., Chibon, P. Y., Oortwijn, M., van der Linden, G. C., Visser, R. G., & Bachem, C. W. (2012). Organ specificity and transcriptional control of metabolic routes revealed by expression QTL profiling of source-sink tissues in a segregating potato population. BMC Plant Biology, 12, 17. http:// doi.org/10.1186/1471-2229-12-17. PMid:22313736.

Komor, A. C., Badran, A. H., & Liu, D. R. (2018). Editing the genome without double-stranded DNA breaks. ACS Chemical Biology, 13(2), 383-388. http://doi.org/10.1021/acschembio.7b00710. PMid:28957631.

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. http://doi.org/10.1038/nature17946. PMid:27096365.

Kreplak, J., Madoui, M. A., Cápal, P., Novák, P., Labadie, K., Aubert, G., Bayer, P. E., Gali, K. K., Syme, R. A., Main, D., Klein, A., Bérard, A., Vrbová, I., Fournier, C., d’Agata, L., Belser, C., Berrabah, W., Toegelová, H., Milec, Z., Vrána, J., Lee, H., Kougbeadjo, A., Térézol, M., Huneau, C., Turo, C. J., Mohellibi, N., Neumann, P., Falque, M., Gallardo, K., McGee, R., Tar’an, B., Bendahmane, A., Aury, J. M., Batley, J., Le Paslier, M. C., Ellis, N., Warkentin, T. D., Coyne, C. J., Salse, J., Edwards, D., Lichtenzveig, J., Macas, J., Doležel, J., Wincker, P., & Burstin, J. (2019). A reference genome for pea provides insight into legume genome evolution. Nature Genetics, 51(9), 1411-1422. http://doi.org/10.1038/ s41588-019-0480-1. PMid:31477930.

Kumar, A., Jaiwal, R., Sreevathsa, R., Chaudhary, D., & Jaiwal, P. K. (2021). Transgenic cowpea plants expressing Bacillus thuringiensis Cry2Aa insecticidal protein imparts resistance to Maruca vitrata legume pod borer. Plant Cell Reports, 40(3), 583-594. http:// doi.org/10.1007/s00299-020-02657-2. PMid:33471196.

Kumar, S., Liu, Z. B., Sanyour-Doyel, N., Lenderts, B., Worden, A., Anand, A., Cho, H.-J., Bolar, J., Harris, C., Huang, L., Xing, A., & Richardson, A. (2022). Efficient gene targeting in soybean using Ochrobactrum haywardense-mediated delivery of a marker-free donor template. Plant Physiology, 189(2), 585-594. http://doi. org/10.1093/plphys/kiac075. PMid:35191500.

Laforest, L. C., & Nadakuduti, S. S. (2022). Advances in delivery mechanisms of CRISPR gene-editing reagents in plants. Frontiers in Genome Editing, 4, 830178. http://doi.org/10.3389/ fgeed.2022.830178. PMid:35141701.

Lamaoui, M., Jemo, M., Datla, R., & Bekkaoui, F. (2018). Heat and drought stresses in crops and approaches for their mitigation. Frontiers in Chemistry, 6, 26. http://doi.org/10.3389/ fchem.2018.00026. PMid:29520357.

Latef, A. A. H. A., & Ahmad, P. (2015). Legumes and breeding under abiotic stress: an overview. In M. M. Azooz, & P. Ahmad (Eds.), Legumes under environmental stress: Yield, improvement and adaptations (pp. 1-20). Wiley. https://doi. org/10.1002/9781118917091.ch1.

Lawrenson, T., Shorinola, O., Stacey, N., Li, C., Østergaard, L., Patron, N., Uauy, C., & Harwood, W. (2015). Induction of targeted, heritable mutations in barley and Brassica oleracea using RNAguided Cas9 nuclease. Genome Biology, 16, 258. http://doi. org/10.1186/s13059-015-0826-7. PMid:26616834.

Le, D. T., Chu, H. D., & Le, N. Q. (2016). Improving nutritional quality of plant proteins through genetic engineering. Current Genomics, 17(3), 220-229. http://doi.org/10.2174/1389202917 666160202215934. PMid:27252589.

LeBlanc, C., Zhang, F., Mendez, J., Lozano, Y., Chatpar, K., Irish, V. F., & Jacob, Y. (2018). Increased efficiency of targeted mutagenesis by CRISPR/Cas9 in plants using heat stress. The Plant Journal, 93(2), 377-386. http://doi.org/10.1111/tpj.13782. PMid:29161464.

Lee, K., & Wang, K. (2023). Strategies for genotype-flexible plant transformation. Current Opinion in Biotechnology, 79, 102848. http://doi.org/10.1016/j.copbio.2022.102848. PMid:36463838.

Lee, M. H., Lee, J., Choi, S. A., Kim, Y. S., Koo, O., Choi, S. H., Ahn, W. S., Jie, E. Y., & Kim, S. W. (2020). Efficient genome editing using CRISPR–Cas9 RNP delivery into cabbage protoplasts via electro-transfection. Plant Biotechnology Reports, 14(6), 695- 702. http://doi.org/10.1007/s11816-020-00645-2.

Lewis, G. P., Schrire, B., Mackinder, B., & Lock, M. (Eds). (2005). Legumes of the world (pp. 127-159). Royal Botanic Gardens Kew.

Li, C., Nguyen, V., Liu, J., Fu, W., Chen, C., Yu, K., & Cui, Y. (2019). Mutagenesis of seed storage protein genes in Soybean using CRISPR/ Cas9. BMC Research Notes, 12(1), 176. http://doi.org/10.1186/ s13104-019-4207-2. PMid:30917862.

Li, G., Liu, R., Xu, R., Varshney, R. K., Ding, H., Li, M., Yan, X., Huang, S., Li, J., Wang, D., Ji, Y., Wang, C., He, J., Luo, Y., Gao, S., Wei, P., Zong, X., & Yang, T. (2023). Development of an Agrobacterium-mediated CRISPR/Cas9 system in pea (Pisum sativum L.). The Crop Journal, 11(1), 132-139. http://doi. org/10.1016/j.cj.2022.04.011.

Li, H. Q., Chen, C., Chen, R. R., Song, X. W., Li, J. N., Zhu, Y. M., & Ding, X. D. (2018). Preliminary analysis of the role of GmSnRK1. 1 and GmSnRK1.2 in the ABA and alkaline stress response of the soybean using the CRISPR/Cas9-based gene double-knockout system. Yi chuan = Hereditas / Zhongguo yi chuan xue hui bian ji, 40(6), 496-507. https://doi.org/10.16288/j.yczz.17-424. PMid: 29959122.

Li, H., Li, J., Shen, Y., Wang, J., & Zhou, D. (2017a). Legume consumption and all-cause and cardiovascular disease mortality. BioMed Research International, 2017, 8450618. http://doi. org/10.1155/2017/8450618. PMid:29230416.

Li, S., Cong, Y., Liu, Y., Wang, T., Shuai, Q., Chen, N., Gai, J., & Li, Y. (2017b). Optimization of Agrobacterium-mediated transformation in soybean. Frontiers in Plant Science, 8, 246. http://doi. org/10.3389/fpls.2017.00246. PMid:28286512.

Li, J. F., Norville, J. E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G. M., & Sheen, J. (2013). Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, 31(8), 688-691. http://doi.org/10.1038/nbt.2654. PMid:23929339.

Li, Z., Liu, Z. B., Xing, A., Moon, B. P., Koellhoffer, J. P., Huang, L., Ward, R. T., Clifton, E., Falco, S. C., & Cigan, A. M. (2015). Cas9-guide RNA directed genome editing in soybean. Plant Physiology, 169(2), 960-970. http://doi.org/10.1104/pp.15.00783. PMid:26294043.

Liang, Z., Chen, K., Li, T., Zhang, Y., Wang, Y., Zhao, Q., Liu, J., Zhang, H., Liu, C., Ran, Y., & Gao, C. (2017). Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nature Communications, 8, 14261. http://doi. org/10.1038/ncomms14261. PMid:28098143.

Liang, Z., Chen, K., Zhang, Y., Liu, J., Yin, K., Qiu, J. L., & Gao, C. (2018). Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nature Protocols, 13(3), 413-430. http://doi.org/10.1038/ nprot.2017.145. PMid:29388938.

Liao, S., Qin, X., Luo, L., Han, Y., Wang, X., Usman, B., Nawaz, G., Zhao, N., Liu, Y., & Li, R. (2019). CRISPR/Cas9-induced mutagenesis of semi-rolled leaf1, 2 confers curled leaf phenotype and drought tolerance by influencing protein expression patterns and ROS scavenging in rice (Oryza sativa L.). Agronomy (Basel), 9(11), 728. http://doi.org/10.3390/agronomy9110728.

Lin, Q., Zong, Y., Xue, C., Wang, S., Jin, S., Zhu, Z., Wang, Y., Anzalone, A. V., Raguram, A., Doman, J. L., Liu, D. R., & Gao, C. (2020). Prime genome editing in rice and wheat. Nature Biotechnology, 38(5), 582-585. http://doi.org/10.1038/s41587- 020-0455-x. PMid:32393904.

Liu, J., Nannas, N. J., Fu, F. F., Shi, J., Aspinwall, B., Parrott, W. A., & Dawe, R. K. (2019a). Genome-scale sequence disruption following biolistic transformation in rice and maize. The Plant Cell, 31(2), 368-383. http://doi.org/10.1105/tpc.18.00613. PMid:30651345.

Liu, W., Rudis, M. R., Cheplick, M. H., Millwood, R. J., Yang, J. P., Ondzighi-Assoume, C. A., Montgomery, G. A., Burris, K. P., Mazarei, M., Chesnut, J. D., & Stewart Junior, C. N. (2020). Lipofection-mediated genome editing using DNA-free delivery of the Cas9/gRNA ribonucleoprotein into plant cells. Plant Cell Reports, 39(2), 245-257. http://doi.org/10.1007/s00299-019- 02488-w. PMid:31728703.

Liu, Y., Wan, X., & Wang, B. (2019). Engineered CRISPRa enables programmable eukaryote-like gene activation in bacteria. Nature Communications, 10(1), 3693. http://doi.org/10.1038/s41467- 019-11479-0. PMid:31451697.

Lonardi, S., Muñoz-Amatriaín, M., Liang, Q., Shu, S., Wanamaker, S. I., Lo, S., Tanskanen, J., Schulman, A. H., Zhu, T., Luo, M.-C., Alhakami, H., Ounit, R., Hasan, A. M., Verdier, J., Roberts, P. A., Santos, J. R.P., Ndeve, A., Doležel, J., Vrána, J., Hokin, S. A., Farmer, A. D., Cannon, S. B., & Close, T. J. (2019). The genome of cowpea (Vigna unguiculata [L.] Walp.). The Plant Journal, 98(5), 767-782. https://onlinelibrary.wiley.com/doi/10.1111/tpj.14349.

Lowder, L. G., Paul, J. W., & Qi, Y. (2017). Multiplexed transcriptional activation or repression in plants using CRISPR-dCas9-based systems. In K. Kaufmann, & B. Mueller-Roeber (Eds.), Plant gene regulatory networks (pp. 167-184). Humana Press. http://doi. org/10.1007/978-1-4939-7125-1_12.

Lowder, L. G., Zhang, D., Baltes, N. J., Paul 3rd, J. W., Tang, X., Zheng, X., Voytas, D. F., Hsieh, T. F., Zhang, Y., & Qi, Y. (2015). A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiology, 169(2), 971-985. http://doi.org/10.1104/pp.15.00636. PMid:26297141.

Lu, Y., Ye, X., Guo, R., Huang, J., Wang, W., Tang, J., Tang, J., Tan, L., Zhu, J.-K., Chu, C., & Qian, Y. (2017). Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Molecular Plant, 10(9), 1242-1245. http://doi.org/10.1016/j. molp.2017.06.007. PMid:28645638.

Ma, X., Zhang, Q., Zhu, Q., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z., Li, H., Lin, Y., Xie, Y., Shen, R., Chen, S., Wang, Z., Chen, Y., Guo, J., Chen, L., Zhao, X., Dong, Z., & Liu, Y.-G. (2015). A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular Plant, 8(8), 1274-1284. http://doi.org/10.1016/j.molp.2015.04.007. PMid:25917172.

Maher, M. F., Nasti, R. A., Vollbrecht, M., Starker, C. G., Clark, M. D., & Voytas, D. F. (2020). Plant gene editing through de novo induction of meristems. Nature Biotechnology, 38(1), 84-89. http://doi.org/10.1038/s41587-019-0337-2. PMid:31844292.

Mahfouz, M. M., Piatek, A., & Stewart Junior, C. N. (2014). Genome engineering via TALENs and CRISPR/Cas9 systems: Challenges and perspectives. Plant Biotechnology Journal, 12(8), 1006-1014. http://doi.org/10.1111/pbi.12256. PMid:25250853.

Makarova, K. S., Aravind, L., Grishin, N. V., Rogozin, I. B., & Koonin, E. V. (2002). A DNA repair system specific for thermophilic Archaea and bacteria predicted by genomic context analysis. Nucleic Acids Research, 30(2), 482-496. http://doi.org/10.1093/nar/30.2.482. PMid:11788711.

Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I., & Koonin, E. V. (2006). A putative RNA-interference-based immune system in prokaryotes: Computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biology Direct, 1(1), 1-26. http://doi.org/10.1186/1745-6150-1-7. PMid:16545108.

Makarova, K. S., Wolf, Y. I., Alkhnbashi, O. S., Costa, F., Shah, S. A., Saunders, S. J., Barrangou, R., Brouns, S. J. J., Charpentier, E., Haft, D. H., Horvath, P., Moineau, S., Mojica, F. J. M., Terns, R. M., Terns, M. P., White, M. F., Yakunin, A. F., Garrett, R. A., van der Oost, J., Backofen, R., & Koonin, E. V. (2015). Backofen, R., & Koonin, E. V. (2105). An updated evolutionary classification of CRISPR–Cas systems. Nature Reviews. Microbiology, 13(11), 722-736. http://doi.org/10.1038/nrmicro3569. PMid:26411297.

Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., & Church, G. M. (2013). RNA-guided human genome engineering via Cas9. Science, 339(6121), 823-826. http://doi. org/10.1126/science.1232033. PMid:23287722.

Malzahn, A. A., Tang, X., Lee, K., Ren, Q., Sretenovic, S., Zhang, Y., Chen, H., Kang, M., Bao, Y., Zheng, X., Deng, K., Zhang, T., Salcedo, V., Wang, K., Zhang, Y., & Qi, Y. (2019). Application of CRISPR-Cas12a temperature sensitivity for improved genome editing in rice, maize, and Arabidopsis. BMC Biology, 17(1), 1-14. http://doi.org/10.1186/s12915-019-0629-5. PMid:30704461.

Maphosa, Y., & Jideani, V. A. (2017). The role of legumes in human nutrition. In M. C. Hueda (Eds.), Functional food-improve health through adequate food. London: IntechOpen. http://doi. org/10.5772/intechopen.69127.

Marraffini, L. A., & Sontheimer, E. J. (2008). CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 322(5909), 1843-1845. http://doi.org/10.1126/ science.1165771. PMid:19095942.

Masson-Boivin, C., & Sachs, J. L. (2018). Symbiotic nitrogen fixation by rhizobia-the roots of a success story. Current Opinion in Plant Biology, 44, 7-15. http://doi.org/10.1016/j.pbi.2017.12.001. PMid:29289792.

Mathan, J., Bhattacharya, J., & Ranjan, A. (2016). Enhancing crop yield by optimizing plant developmental features. Development, 143(18), 3283-3294. http://doi.org/10.1242/dev.134072. PMid:27624833.

Meng, X., Yu, H., Zhang, Y., Zhuang, F., Song, X., Gao, S., Gao, C., & Li, J. (2017b). Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Molecular Plant, 10(9), 1238-1241. http://doi.org/10.1016/j.molp.2017.06.006. PMid:28645639.

Meng, Y., Hou, Y., Wang, H., Ji, R., Liu, B., Wen, J., Niu, L., & Lin, H. (2017b). Targeted mutagenesis by CRISPR/Cas9 system in the model legume Medicago truncatula. Plant Cell Reports, 36(2), 371- 374. http://doi.org/10.1007/s00299-016-2069-9. PMid:27834007.

Meng, Y., Liu, H., Wang, H., Liu, Y., Zhu, B., Wang, Z., Hou, Y., Zhang, P.,Wen, J., Yang, H., Mysore, K. S., Chen, J., Tadege, M., Niu, L., Lin, H. (2019). HEADLESS, a WUSCHEL homolog, uncovers novel aspects of shoot meristem regulation and leaf blade development in Medicago truncatula. Journal of Experimental Botany, 70(1), 149-163. https://doi.org/10.1093/jxb/ery346.

Metje-Sprink, J., Menz, J., Modrzejewski, D., & Sprink, T. (2019). DNAfree genome editing: Past, present and future. Frontiers in Plant Science, 1957, 1957. http://doi.org/10.3389/fpls.2018.01957. PMid:30693009.

Mhadhbi, H., Mylona, P. V., & Polidoros, A. N. (2015). Legume-rhizobia symbiotic performance under abiotic stresses: Factors influencing tolerance behavior. In M. M. Azooz, & P. Ahmad (Eds.), Legumes under environmental stress: Yield, improvement and adaptations (pp. 125-131). Wiley. https://doi.org/10.1002/9781118917091. ch8.

Michno, J. M., Wang, X., Liu, J., Curtin, S. J., Kono, T. J., & Stupar, R. M. (2015). CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops and Food: Biotechnology in Agriculture and the Food Chain, 6(4), 243-252. http://doi.org/10.1080/21645698.2015.1 106063. PMid:26479970.

Miller, S. S., Dornbusch, M. R., Farmer, A. D., Huertas, R., GutierrezGonzalez, J. J., Young, N. D., Samac, D. A., & Curtin, S. J. (2022). Alfalfa (Medicago sativa L.) pho2 mutant plants hyperaccumulate phosphate. G3, 12(6), jkac096. https://doi.org/10.1093/ g3journal/jkac096.

Mishra, R., Joshi, R. K., & Zhao, K. (2020). Base editing in crops: Current advances, limitations and future implications. Plant Biotechnology Journal, 18(1), 20-31. http://doi.org/10.1111/ pbi.13225. PMid:31365173.

Mizuno, A., & Okada, Y. (2019). Biological characterization of expression quantitative trait loci (eQTLs) showing tissue-specific opposite directional effects. European Journal of Human Genetics, 27(11), 1745-1756. http://doi.org/10.1038/s41431-019-0468-4. PMid:31296926.

Mohammed, S., Abd Samad, A., & Rahmat, Z. (2019). Agrobacteriummediated transformation of rice: Constraints and possible solutions. Rice Science, 26(3), 133-146. http://doi.org/10.1016/j. rsci.2019.04.001.

Mojica, F. J. M., Ferrer, C., Juez, G., & Rodríguez-Valera, F. (1995). Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Molecular Microbiology, 17(1), 85-93. http://doi. org/10.1111/j.1365-2958.1995.mmi_17010085.x. PMid:7476211.

Mojica, F. J., Díez-Villaseñor, C., García-Martínez, J., & Soria, E. (2005). Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of Molecular Evolution, 60(2), 174-182. http://doi.org/10.1007/s00239-004- 0046-3. PMid:15791728.

Mojica, F. J., Díez-Villaseñor, C., Soria, E., & Juez, G. (2000). Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Molecular Microbiology, 36(1), 244-246. http://doi.org/10.1046/j.1365- 2958.2000.01838.x. PMid:10760181.

Mojica, F. J., Juez, G., & Rodriguez-Valera, F. (1993). Transcription at different salinities of Haloferax mediterranei sequences adjacent to partially modified PstI sites. Molecular Microbiology, 9(3), 613-621. http://doi.org/10.1111/j.1365-2958.1993.tb01721.x. PMid:8412707.

Mougiakos, I., Bosma, E. F., Ganguly, J., Van Der Oost, J., & Van Kranenburg, R. (2018). Hijacking CRISPR-Cas for high-throughput bacterial metabolic engineering: Advances and prospects. Current Opinion in Biotechnology, 50, 146-157. http://doi.org/10.1016/j. copbio.2018.01.002. PMid:29414054.

Mousavi-Derazmahalleh, M., Bayer, P. E., Hane, J. K., Valliyodan, B., Nguyen, H. T., Nelson, M. N., Erskine, W., Varshney, R. K., Papa, R., & Edwards, D. (2019). Adapting legume crops to climate change using genomic approaches. Plant, Cell & Environment, 42(1), 6-19. http://doi.org/10.1111/pce.13203. PMid:29603775.

Mudryj, A. N., Yu, N., & Aukema, H. M. (2014). Nutritional and health benefits of pulses. Applied Physiology, Nutrition, and Metabolism, 39(11), 1197-1204. http://doi.org/10.1139/apnm2013-0557. PMid:25061763.

Muzquiz, M., Varela, A., Burbano, C., Cuadrado, C., Guillamón, E., & Pedrosa, M. M. (2012). Bioactive compounds in legumes: Pronutritive and antinutritive actions. Implications for nutrition and health. Phytochemistry Reviews, 11(2), 227-244. http://doi. org/10.1007/s11101-012-9233-9.

Myskja, B. K., & Myhr, A. I. (2020). Non-safety assessments of genome-edited organisms: Should they be included in regulation? Science and Engineering Ethics, 26(5), 2601-2627. http://doi. org/10.1007/s11948-020-00222-4. PMid:32424723.

Nadeem, M., Li, J., Yahya, M., Wang, M., Ali, A., Cheng, A., Wang, X., & Ma, C. (2019). Grain legumes and fear of salt stress: Focus on mechanisms and management strategies. International Journal of Molecular Sciences, 20(4), 799. http://doi.org/10.3390/ ijms20040799. PMid:30781763.

Nakayasu, M., Akiyama, R., Lee, H. J., Osakabe, K., Osakabe, Y., Watanabe, B., Sugimoto, Y., Umemoto, N., Saito, K., Muranaka, T., & Mizutani, M. (2018). Generation of α-solanine-free hairy roots of potato by CRISPR/Cas9 mediated genome editing of the St16DOX gene. Plant Physiology and Biochemistry, 131, 70-77. http://doi.org/10.1016/j.plaphy.2018.04.026. PMid:29735370.

Nanjareddy, K., Arthikala, M. K., Blanco, L., Arellano, E. S., & Lara, M. (2016). Protoplast isolation, transient transformation of leaf mesophyll protoplasts and improved Agrobacterium-mediated leaf disc infiltration of Phaseolus vulgaris: Tools for rapid gene expression analysis. BMC Biotechnology, 16(1), 53. http://doi. org/10.1186/s12896-016-0283-8. PMid:27342637.

Naves, E. R., de Ávila Silva, L., Sulpice, R., Araújo, W. L., Nunes-Nesi, A., Peres, L. E., & Zsögön, A. (2019). Capsaicinoids: Pungency beyond Capsicum. Trends in Plant Science, 24(2), 109-120. http:// doi.org/10.1016/j.tplants.2018.11.001. PMid:30630668.

Nedumaran, S., Abinaya, P., Jyosthnaa, P., Shraavya, B., Rao, P., & Bantilan, C. (2015). Grain legumes production, consumption and trade trends in developing countries (Working Paper Series, No. 60). CGIAR.

Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J. D., & Kamoun, S. (2013). Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nature Biotechnology, 31(8), 691-693. http://doi.org/10.1038/nbt.2655. PMid:23929340.

Niazian, M., Belzile, F., & Torkamaneh, D. (2022). CRISPR/Cas9 in planta hairy root transformation: A powerful platform for functional analysis of root traits in soybean. Plants, 11(8), 1044. http://doi.org/10.3390/plants11081044. PMid:35448772.

Okuley, J., Lightner, J., Feldmann, K., Yadav, N., Lark, E., & Browse, J. (1994). Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. The Plant Cell, 6(1), 147-158. http://doi.org/10.1105/tpc.6.1.147. PMid:7907506.

Orlich, M. J., Jaceldo-Siegl, K., Sabaté, J., Fan, J., Singh, P. N., & Fraser, G. E. (2014). Patterns of food consumption among vegetarians and non-vegetarians. British Journal of Nutrition, 112(10), 1644-1653. http://doi.org/10.1017/S000711451400261X. PMid:25247790.

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. http://doi.org/10.1111/pbi.13006. PMid:30183125.

Osipova, M. A., Dolgikh, E. A., & Lutova, L. A. (2011). Peculiarities of meristem-specific WOX5 gene expression during nodule organogenesis in legumes. Russian Journal of Developmental Biology, 42(4), 226-237. http://doi.org/10.1134/ S1062360411010085.

Ott, T., van Dongen, J. T., Günther, C., Krusell, L., Desbrosses, G., Vigeolas, H., Bock, V., Czechowski, T., Geigenberger, P., & Udvardi, M. K. (2005). Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Current Biology, 15(6), 531-535. http://doi. org/10.1016/j.cub.2005.01.042. PMid:15797021.

Ozyigit, I. I., & Kurtoglu, K. Y. (2020). Particle bombardment technology and its applications in plants. Molecular Biology Reports, 47(12), 9831-9847. http://doi.org/10.1007/s11033- 020-06001-5. PMid:33222118.

Paes de Melo, B., Lourenço-Tessutti, I. T., Morgante, C. V., Santos, N. C., Pinheiro, L. B., de Jesus Lins, C. B., Silva, M. C. M., Macedo, L. L. P., Fontes, E. P. B., & Grossi-de-Sa, M. F. (2020). Soybean embryonic axis transformation: Combining biolistic and Agrobacterium-mediated protocols to overcome typical complications of in vitro plant regeneration. Frontiers in Plant Science, 11, 1228. http://doi.org/10.3389/fpls.2020.01228. PMid:32903423.

Pandey, M. K., Roorkiwal, M., Singh, V. K., Ramalingam, A., Kudapa, H., Thudi, M., Chitikineni, A., Rathore, A., & Varshney, R. K. (2016). Emerging genomic tools for legume breeding: Current status and future prospects. Frontiers in Plant Science, 7, 455. http://doi.org/10.3389/fpls.2016.00455. PMid:27199998.

Pareddy, D., Chennareddy, S., Anthony, G., Sardesai, N., Mall, T., Minnicks, T., Karpova, O., Clark, L., Griffin, D., Bishop, B., Shumway, N., Samuel, P., Smith, K., & Sarria, R. (2020). Improved soybean transformation for efficient and high throughput transgenic production. Transgenic Research, 29(3), 267-281. http://doi.org/10.1007/s11248-020-00198-8. PMid:32303980.

Patil, G. B., Stupar, R. M., & Zhang, F. (2022). Protoplast isolation, transfection, and gene editing for soybean soybeans (Glycine max). In K. Wang, & F. Zhang (Eds.), Protoplast technology: Methods and Protocols (pp. 173-186). Springer. https://doi. org/10.1007/978-1-0716-2164-6_13.

Phillips, A. L. (2016). Genetic control of gibberellin metabolism and signalling in crop improvement. In P. Hedden, & S. G. Thomas (Eds.), Annual Plant Reviews (Vol. 49: Gibberellins, The, pp. 405-430). John Wiley & Sons, Ltd. https://doi. org/10.1002/9781119210436.ch13.

Piatek, A., Ali, Z., Baazim, H., Li, L., Abulfaraj, A., Al-Shareef, S., Aouida, M., & Mahfouz, M. M. (2015). RNA-guided transcriptional regulation in planta via synthetic dC as9-based transcription factors. Plant Biotechnology Journal, 13(4), 578-589. http:// doi.org/10.1111/pbi.12284. PMid:25400128.

Polowick, P. L., & Yan, W. (2023). A protocol for Agrobacteriummediated genetic transformation of Lens culinaris Medik (lentil). Plant Cell, Tissue and Organ Culture, 152(3), 605-618. http:// doi.org/10.1007/s11240-022-02434-x.

Pourcel, C., Salvignol, G., & Vergnaud, G. (2005). CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA and provide additional tools for evolutionary studies. Microbiology, 151(Pt 3), 653-663. http://doi.org/10.1099/ mic.0.27437-0. PMid:15758212.

Qian, L., Jin, H., Yang, Q., Zhu, L., Yu, X., Fu, X., Zhao, M., & Yuan, F. (2022). A sequence variation in GmBADH2 enhances soybean aroma and is a functional marker for improving soybean flavor. International Journal of Molecular Sciences, 23(8), 4116. http:// doi.org/10.3390/ijms23084116. PMid:35456933.

Quareshy, M., Prusinska, J., Li, J., & Napier, R. (2018). A cheminformatics review of auxins as herbicides. Journal of Experimental Botany, 69(2), 265-275. http://doi.org/10.1093/ jxb/erx258. PMid:28992122.

Ran, Y., Liang, Z., & Gao, C. (2017). Current and future editing reagent delivery systems for plant genome editing. Science China. Life Sciences, 60(5), 490-505. http://doi.org/10.1007/ s11427-017-9022-1. PMid:28527114.

Razzaq, A., Saleem, F., Kanwal, M., Mustafa, G., Yousaf, S., Arshad, H. M. I., Hameed, M. K., Khan, M. S., & Joyia, F. A. (2019). Modern trends in plant genome editing: An inclusive review of the CRISPR/ Cas9 toolbox. International Journal of Molecular Sciences, 20(16), 4045. http://doi.org/10.3390/ijms20164045. PMid:31430902.

Rehman, H. M., Cooper, J. W., Lam, H. M., & Yang, S. H. (2019). Legume biofortification is an underexploited strategy for combatting hidden hunger. Plant, Cell & Environment, 42(1), 52-70. http://doi.org/10.1111/pce.13368. PMid:29920691.

Riascos, J. J., Weissinger, A. K., Weissinger, S. M., & Burks, A. W. (2010). Hypoallergenic legume crops and food allergy: Factors affecting feasibility and risk. Journal of Agricultural and Food Chemistry, 58(1), 20-27. http://doi.org/10.1021/jf902526y. PMid:19921800.

Roca Paixão, J. F., Gillet, F. X., Ribeiro, T. P., Bournaud, C., LourençoTessutti, I. T., Noriega, D. D., de Melo, B. P., de Almeida-Engler, J., & Grossi-de-Sa, M. F. (2019). Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a Histone AcetylTransferase. Scientific Reports, 9(1), 8080. http://doi. org/10.1038/s41598-019-44571-y. PMid:31147630.

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. http://doi.org/10.1016/j.cell.2017.08.030. PMid:28919077.

Roy, S., Liu, W., Nandety, R. S., Crook, A., Mysore, K. S., Pislariu, C. I., Frugoli, J., Dickstein, R., & Udvardi, M. K. (2020). Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. The Plant Cell, 32(1), 15-41. http://doi. org/10.1105/tpc.19.00279. PMid:31649123.

Rustgi, S., Naveed, S., Windham, J., Zhang, H., & Demirer, G. S. (2022). Plant biomacromolecule delivery methods in the 21st century. Frontiers in Genome Editing, 4, 1011934. http://doi. org/10.3389/fgeed.2022.1011934. PMid:36311974.

Sack, L., & Scoffoni, C. (2013). Leaf venation: Structure, function, development, evolution, ecology and applications in the past, present and future. The New Phytologist, 198(4), 983-1000. http://doi.org/10.1111/nph.12253. PMid:23600478.

Sadhu, S. K., Jogam, P., Gande, K., Banoth, R., Penna, S., & Peddaboina, V. (2022). Optimization of different factors for an Agrobacterium-mediated genetic transformation system using embryo axis explants of chickpea (Cicer arietinum L.). Journal of Plant Biotechnology, 49(1), 61-73. http://doi.org/10.5010/ JPB.2022.49.1.061.

Sandhya, D., Jogam, P., Allini, V. R., Abbagani, S., & Alok, A. (2020). The present and potential future methods for delivering CRISPR/ Cas9 components in plants. Journal of Genetic Engineering and Biotechnology, 18(1), 1-11. http://doi.org/10.1186/s43141-020- 00036-8. PMid:32638190.

Santamaria, M. E., Arnaiz, A., Gonzalez-Melendi, P., Martinez, M., & Diaz, I. (2018). Plant perception and short-term responses to phytophagous insects and mites. International Journal of Molecular Sciences, 19(5), 1356. http://doi.org/10.3390/ ijms19051356. PMid:29751577.

Sarker, R. H., Das, S. K., Shethi, K. J., & Hoque, M. I. (2019). Genetic transformation. In M. Singh (Ed.), Lentils (pp. 141-202). Academic Press. http://doi.org/10.1016/B978-0-12-813522-8.00008-X

Sarrocco, S., Herrera-Estrella, A., & Collinge, D. B. (2020). Plant disease management in the post-genomic era: From functional genomics to genome editing. Frontiers in Microbiology, 11, 107. http://doi.org/10.3389/fmicb.2020.00107. PMid:32117135.

Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., Kato, T., Nakao, M., Sasamoto, S., Watanabe, A., Ono, A., Kawashima, K., Fujishiro, T., Katoh, M., Kohara, M., Kishida, Y., Minami, C., Nakayama, S., Nakazaki, N., Shimizu, Y., Shinpo, S., Takahashi, C., Wada, T., Yamada, M., Ohmido, N., Hayashi, M., Fukui, K., Baba, T., Nakamichi, T., Mori, H., & Tabata, S. (2008). Genome structure of the legume, Lotus japonicus. DNA Research, 15(4), 227-239. http://doi.org/10.1093/dnares/dsn008. PMid:18511435.

Schlueter, J. A., Vasylenko-Sanders, I. F., Deshpande, S., Yi, J., Siegfried, M., Roe, B. A., Schlueter, S. D., Scheffler, B. E., & Shoemaker, R. C. (2007). The FAD2 gene family of soybean: Insights into the structural and functional divergence of a paleopolyploid genome. Crop Science, 47(S1), S-14. http://doi.org/10.2135/ cropsci2006.06.0382tpg.

Schmutz, J., Cannon, S. B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D. L., Song, Q., Thelen, J. J., Cheng, J., Xu, D., Hellsten, U., May, G. D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M. K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., FutrellGriggs, M., Abernathy, B., Du, J., Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X. C., Shinozaki, K., Nguyen, H. T., Wing, R. A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R. C., & Jackson, S. A. (2010). Genome sequence of the palaeopolyploid soybean. Nature, 463(7278), 178-183. http://doi.org/10.1038/nature08670. PMid:20075913.

Schmutz, J., McClean, P. E., Mamidi, S., Wu, G. A., Cannon, S. B., Grimwood, J., Jenkins, J., Shu, S., Song, Q., Chavarro, C., TorresTorres, M., Geffroy, V., Moghaddam, S. M., Gao, D., Abernathy, B., Barry, K., Blair, M., Brick, M. A., Chovatia, M., Gepts, P., Goodstein, D. M., Gonzales, M., Hellsten, U., Hyten, D. L., Jia, G., Kelly, J. D., Kudrna, D., Lee, R., Richard, M. M., Miklas, P. N., Osorno, J. M., Rodrigues, J., Thareau, V., Urrea, C. A., Wang, M., Yu, Y., Zhang, M., Wing, R. A., Cregan, P. B., Rokhsar, D. S., & Jackson, S. A. (2014). A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics, 46(7), 707-713. http://doi.org/10.1038/ng.3008. PMid:24908249.

Schreinemachers, P., Srinivasan, R., Wu, M. H., Bhattarai, M., Patricio, R., Yule, S., Quang, V. H., & Hop, B. T. H. (2014). Safe and sustainable management of legume pests and diseases in Thailand and Vietnam: A situational analysis. International Journal of Tropical Insect Science, 34(2), 88-97. http://doi.org/10.1017/ S174275841400023X.

Sehaole, E. K. M. (2022). Genetic transformation in agro-economically important legumes. In J. C. Jimenez-Lopez, & A. Clemente (Eds.), Legumes research (Vol. 1). London: IntechOpen. https://doi. org//10.5772/intechopen.101262.

Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, Z., Liu, J., Xi, J., Qiu, J. L., & Gao, C. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology, 31(8), 686-688. http://doi.org/10.1038/nbt.2650. PMid:23929338.

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. http://doi.org/10.1111/pbi.12603. PMid:27442592.

Shinozaki, K., & Yamaguchi-Shinozaki, K. (2007). Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany, 58(2), 221-227. http://doi.org/10.1093/ jxb/erl164. PMid:17075077.

Shmakov, S., Smargon, A., Scott, D., Cox, D., Pyzocha, N., Yan, W., Abudayyeh, O. O., Gootenberg, J. S., Makarova, K. S., Wolf, Y. I., Severinov, K., Zhang, F., & Koonin, E. V. (2017). Diversity and evolution of class 2 CRISPR–Cas systems. Nature Reviews. Microbiology, 15(3), 169-182. http://doi.org/10.1038/ nrmicro.2016.184. PMid:28111461.

Shrestha, A., Khan, A., & Dey, N. (2018). cis – trans Engineering: Advances and Perspectives on Customized Transcriptional Regulation in Plants. Molecular Plant, 11(7), 886-898. http:// doi.org/10.1016/j.molp.2018.05.008. PMid:29859265.

Shu, H., Luo, Z., Peng, Z., & Wang, J. (2020). The application of CRISPR/Cas9 in hairy roots to explore the functions of AhNFR1 and AhNFR5 genes during peanut nodulation. BMC Plant Biology, 20(1), 417. http://doi.org/10.1186/s12870-020-02614-x. PMid:32894045.

Simkin, A. J., Mcausland, L., Headland, L. R., Lawson, T., & Raines, C. A. (2015). Multigene manipulation of photosynthetic carbon assimilation increases CO 2 fixation and biomass yield in tobacco. Journal of Experimental Botany, 66(13), 4075-4090. https://doi. org/10.1093/jxb/erv204.

Singh, P., Shukla, A., Tiwari, N. N., Ansari, J., Thakur, S., Patil, P. G., Rathore, M., Verma, O. P., Singh, N. P., & Das, A. (2022). Routine and efficient in vitro regeneration system amenable to biolistic particle delivery in chickpea (Cicer arietinum L.). Plant Cell, Tissue and Organ Culture, 148(3), 699-711. http://doi. org/10.1007/s11240-022-02230-7.

Smyth, S. J. (2019). Global status of the regulation of genome editing technologies. Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 14(21), 1-6. http:// doi.org/10.1079/PAVSNNR201914021.

Soltani, N., Dille, J. A., Burke, I. C., Everman, W. J., VanGessel, M. J., Davis, V. M., & Sikkema, P. H. (2016). Potential corn yield losses from weeds in North America. Weed Technology, 30(4), 979-984. http://doi.org/10.1614/WT-D-16-00046.1.

Somers, D. A., Samac, D. A., & Olhoft, P. M. (2003). Recent advances in legume transformation. Plant Physiology, 131(3), 892-899. http://doi.org/10.1104/pp.102.017681. PMid:12644642.

Soumare, A., Diedhiou, A. G., Thuita, M., Hafidi, M., Ouhdouch, Y., Gopalakrishnan, S., & Kouisni, L. (2020). Exploiting biological nitrogen fixation: A route towards a sustainable agriculture. Plants, 9(8), 1011. http://doi.org/10.3390/plants9081011. PMid:32796519.

Stacey, G. (2007). The Rhizobium-legume nitrogen-fixing symbiosis. In H. Bothe, S. J. Ferguson, & W. E. Newton (Eds.), Biology of the nitrogen cycle (pp. 147-163). Elsevier. http://doi.org/10.1016/ B978-044452857-5.50011-4.

Stagnari, F., Maggio, A., Galieni, A., & Pisante, M. (2017). Multiple benefits of legumes for agriculture sustainability: An overview. Chemical and Biological Technologies in Agriculture, 4(1), 1-13. http://doi.org/10.1186/s40538-016-0085-1.

Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., & Parniske, M. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature, 417(6892), 959-962. http://doi. org/10.1038/nature00841. PMid:12087405. Subburaj, S., Zanatta, C. B., Nunn, J. A., Hoepers, A. M., Nodari, R. O., & Agapito-Tenfen, S. Z. (2022). A DNA-free editing platform for genetic screens in soybean via CRISPR/Cas9 ribonucleoprotein delivery. Frontiers in Plant Science, 13, 939997. http://doi. org/10.3389/fpls.2022.939997. PMid:35903231.

Sun, X., Hu, Z., Chen, R., Jiang, Q., Song, G., Zhang, H., & Xi, Y. (2015). Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Scientific Reports, 5(1), 10342. http://doi.org/10.1038/ srep10342. PMid:26022141.

Sun, Y., Li, J., & Xia, L. (2016). Precise genome modification via sequence-specific nucleases-mediated gene targeting for crop improvement. Frontiers in Plant Science, 7, 1928. http://doi. org/10.3389/fpls.2016.01928. PMid:28066481.

Svitashev, S., Young, J. K., Schwartz, C., Gao, H., Falco, S. C., & Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiology, 169(2), 931-945. http://doi.org/10.1104/ pp.15.00793. PMid:26269544.

Tang, F., Yang, S., Liu, J., & Zhu, H. (2016). Rj4, a gene controlling nodulation specificity in soybeans, encodes a thaumatinlike protein but not the one previously reported. Plant Physiology, 170(1), 26-32. http://doi.org/10.1104/pp.15.01661. PMid:26582727.

Tang, X., Lowder, L. G., Zhang, T., Malzahn, A. A., Zheng, X., Voytas, D. F., Zhong, Z., Chen, Y., Ren, Q., Li, Q., Kirkland, E. R., Zhang, Y., & Qi, Y. (2017). A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nature Plants, 3, 17018. http://doi.org/10.1038/nplants.2017.18. PMid:28211909.

Tchetvertakov, G. (2019) Australia approves cutting-edge CRISPR gene editing technology. https://smallcaps.com.au/australiaapproves-cutting-edge-crispr-gene-editing-technology/ Tharanathan, R. N., & Mahadevamma, S. (2003). Grain legumes-a boon to human nutrition. Trends in Food Science & Technology, 14(12), 507-518. http://doi.org/10.1016/j.tifs.2003.07.002.

The Legume Phylogeny Working Group. (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon. 66(1), 44-77. https://doi. org/10.12705/661.3.

Tichá, M., Illésová, P., Hrbáčková, M., Basheer, J., Novák, D., Hlaváčková, K., Šamajová, O., Niehaus, K., Ovečka, M., & Šamaj, J. (2020). Tissue culture, genetic transformation, interaction with beneficial microbes, and modern bio-imaging techniques in alfalfa research. Critical Reviews in Biotechnology, 40(8), 1265-1280. http://doi.org/10.1080/07388551.2020.1814689. PMid:32942912.

Tiwari, P., Indoliya, Y., Chauhan, A. S., Pande, V., & Chakrabarty, D. (2020). Over-expression of rice R1-type MYB transcription factor confers different abiotic stress tolerance in transgenic Arabidopsis. Ecotoxicology and Environmental Safety, 206, 111361. http:// doi.org/10.1016/j.ecoenv.2020.111361. PMid:32987264.

Tiwari, R., Singh, A. K., & Rajam, M. V. (2022). Improved and reliable plant regeneration and Agrobacterium-mediated genetic transformation in soybean (Glycine max L.). Journal of Crop Science and Biotechnology, 26, 275-284. http://doi.org/10.1007/ s12892-022-00179-9.

Trinh, D. D., Le, N. T., Bui, T. P., Le, T. N. T., Nguyen, C. X., Chu, H. H., & Do, P. T. (2022). A sequential transformation method for validating soybean genome editing by CRISPR/Cas9 system. Saudi Journal of Biological Sciences, 29(10), 103420. http://doi. org/10.1016/j.sjbs.2022.103420. PMid:36060110.

Triozzi, P. M., Schmidt, H. W., Dervinis, C., Kirst, M., & Conde, D. (2021). Simple, efficient and open-source CRISPR/Cas9 strategy for multi-site genome editing in Populus tremula× alba. Tree Physiology, 41(11), 2216-2227. http://doi.org/10.1093/treephys/ tpab066. PMid:33960379.

Turnbull, C., Lillemo, M., & Hvoslef-Eide, T. A. (2021). Global regulation of genetically modified crops amid the gene edited crop boom–a review. Frontiers in Plant Science, 12, 630396. http:// doi.org/10.3389/fpls.2021.630396. PMid:33719302.

United Nations. (2022). World Population Prospects 2022. Department of Economic and Social Affairs Population Dynamics. https:// population.un.org/wpp/

USDA Aphis. (2020). 7 CFR Parts 330, 340, and 372: RIN 0579-AE47. USDA APHIS.

Valdisser, P. A., Pereira, W. J., Almeida Filho, J. E., Müller, B. S., Coelho, G. R., de Menezes, I. P., Vianna, J. P. G., Zucchi, M. I., Lanna, A. C., Coelho, A. S. G., de Oliveira, J. P., Moraes, A. C., Brondani, C., & Vianello, R. P. (2017). In-depth genome characterization of a Brazilian common bean core collection using DArTseq high-density SNP genotyping. BMC Genomics, 18(1), 423. http://doi.org/10.1186/s12864-017-3805-4. PMid:28558696.

Valentine, A. J., Benedito, V. A., & Kang, Y. (2011). Legume nitrogen fixation and soil abiotic stress: From physiology to genomics and beyond. Annual Plant Reviews, 42, 207-248. http://doi. org/10.1002/9781119312994.apr0456.

van Dijk, M., Morley, T., Rau, M. L., & Saghai, Y. (2021). A metaanalysis of projected global food demand and population at risk of hunger for the period 2010–2050. Nature Food, 2(7), 494-501. http://doi.org/10.1038/s43016-021-00322-9. PMid:37117684.

van Kregten, M., de Pater, S., Romeijn, R., van Schendel, R., Hooykaas, P. J., & Tijsterman, M. (2016). T-DNA integration in plants results from polymerase-θ-mediated DNA repair. Nature Plants, 2(11), 16164. http://doi.org/10.1038/nplants.2016.164. PMid:27797358.

van Loon, P., & Van Wassenhove, L. N. (2018). Assessing the economic and environmental impact of remanufacturing: A decision support tool for OEM suppliers. International Journal of Production Research, 56(4), 1662-1674. http://doi.org/10.1080/0020754 3.2017.1367107.

Varshney, R. K. (2016). Emerging genomic tools for legume breeding: Current status and future prospects. Frontiers in Plant Science, 7, 455. PMid:27199998.

Varshney, R. K., Chen, W., Li, Y., Bharti, A. K., Saxena, R. K., Schlueter, J. A., Donoghue, M. T., Azam, S., Fan, G, Whaley, A. M., Farmer, A. D., Sheridan, J., Iwata, A., Tuteja, R., Penmetsa, R. V., Wu, W., Upadhyaya, H. D., Yang, S. P., Shah, T., Saxena, K. B., Michael, T., McCombie, W. R., Yang, B., Zhang, G., Yang, H., Wang, J., Spillane, C., Cook, D. R., May, G. D., Xu, X., & Jackson, S. A. (2011). Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nature Biotechnology, 30(1), 83-89. http://doi.org/10.1038/ nbt.2022. PMid:22057054.

Varshney, R. K., Kudapa, H., Pazhamala, L., Chitikineni, A., Thudi, M., Bohra, A., Gaur, P. M., Janila, P., Fikre, A., Kimurto, P., & Ellis, N. (2015). Translational genomics in agriculture: Some examples in grain legumes. Critical Reviews in Plant Sciences, 34(1-3), 169-194. http://doi.org/10.1080/07352689.2014.897909.

Varshney, R. K., Song, C., Saxena, R. K., Azam, S., Yu, S., Sharpe, A. G., Cannon, S., Baek, J., Rosen, B. D., Tar’an, B., Millan, T., Zhang, X., Ramsay, L D., Iwata, A., Wang, Y., Nelson, W., Farmer, A. D., Gaur, P. M., Soderlund, C., Penmetsa, R. V., Xu, C., Bharti, A. K., He, W., Winter, P., Zhao, S., Hane, J. K., Carrasquilla-Garcia, N., Condie, J. A., Upadhyaya, H. D., Luo, M. C., Thudi, M., Gowda, C. L., Singh, N. P., Lichtenzveig, J., Gali, K. K., Rubio, J., Nadarajan, N., Dolezel, J., Bansal, K. C., Xu, X., Edwards, D., Zhang, G., Kahl, G., Gil, J., Singh, K. B., Datta, S. K., Jackson, S. A., Wang, J., & Cook, D. R. (2013). Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nature Biotechnology, 31(3), 240-246. http:// doi.org/10.1038/nbt.2491. PMid:23354103.

Verma, A. K., Kumar, S., Das, M., & Dwivedi, P. D. (2013). A comprehensive review of legume allergy. Clinical Reviews in Allergy & Immunology, 45(1), 30-46. http://doi.org/10.1007/ s12016-012-8310-6. PMid:22555630.

Voytas, D. F., & Gao, C. (2014). Precision genome engineering and agriculture: Opportunities and regulatory challenges. PLoS Biology, 12(6), e1001877. http://doi.org/10.1371/journal.pbio.1001877. PMid:24915127.

Wang, L., Rubio, M. C., Xin, X., Zhang, B., Fan, Q., Wang, Q., Ning, G., Becana, M., & Duanmu, D. (2019). CRISPR/Cas9 knockout of leghemoglobin genes in Lotus japonicus uncovers their synergistic roles in symbiotic nitrogen fixation. The New Phytologist, 224(2), 818-832. http://doi.org/10.1111/nph.16077. PMid:31355948.

Wang, L., Wang, L., Tan, Q., Fan, Q., Zhu, H., Hong, Z., Zhang, Z., & Duanmu, D. (2016). Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus using CRISPR-Cas9. Frontiers in Plant Science, 7, 1333. http://doi.org/10.3389/ fpls.2016.01333. PMid:27630657.

Wang, Y., Zhao, J., Lu, W., & Deng, D. (2017). Gibberellin in plant height control: Old player, new story. Plant Cell Reports, 36(3), 391-398. http://doi.org/10.1007/s00299-017-2104-5. PMid:28160061.

Wani, A. K., Akhtar, N., & Shukla, S. (2022). CRISPR/Cas9: Regulations and challenges for law enforcement to combat its dual-use. Forensic Science International, 334, 111274. http:// doi.org/10.1016/j.forsciint.2022.111274. PMid:35316773.

Weber, A. P., & Bar-Even, A. (2019). Update: Improving the efficiency of photosynthetic carbon reactions. Plant Physiology, 179(3), 803-812. http://doi.org/10.1104/pp.18.01521. PMid:30610109.

Weiner, J. (2019). Looking in the wrong direction for higher-yielding crop genotypes. Trends in Plant Science, 24(10), 927-933. http:// doi.org/10.1016/j.tplants.2019.07.001. PMid:31358472.

World Cancer Research Fund, & American Institute for Cancer Research. (2014). Diet, nutrition, physical activity, and cancer: A global perspective (Third Expert Report. 2014). WHO Press, World Cancer Report. http://www.aicr.org/cancer-research/ dietandcancerreport/

Wu, F. H., Shen, S. C., Lee, L. Y., Lee, S. H., Chan, M. T., & Lin, C. S. (2009). Tape-Arabidopsis Sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods, 5(1), 1-10. http:// doi.org/10.1186/1746-4811-5-16. PMid:19930690.

Wu, F., & Hanzawa, Y. (2018). A simple method for isolation of soybean protoplasts and application to transient gene expression analyses. JoVE (Journal of Visualized Experiments), (131), e57258. https://doi.org/10.3791/57258.

Xing, H.-L., Dong, L., Wang, Z.-P., Zhang, H.-Y., Han, C.-Y., Liu, B., Wang, X.-C., & Chen, Q.-J. (2014). A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology, 14(1), 327. http://doi.org/10.1186/s12870-014-0327-y. PMid:25432517.

Xiong, L., Li, C., Li, H., Lyu, X., Zhao, T., Liu, J., Zuo, Z., & Liu, B. (2019). A transient expression system in soybean mesophyll protoplasts reveals the formation of cytoplasmic GmCRY1 photobody-like structures. Science China. Life Sciences, 62(8), 1070-1077. http://doi.org/10.1007/s11427-018-9496-5. PMid:30929191.

Xu, H., Guo, Y., Qiu, L., & Ran, Y. (2022). Progress in soybean genetic transformation over the last decade. Frontiers in Plant Science, 13, 900318. http://doi.org/10.3389/fpls.2022.900318. PMid:35755694.

Yang, Z., Du, H., Xing, X., Li, W., Kong, Y., Li, X., & Zhang, C. (2022). A small heat shock protein, GmHSP17. 9, from nodule confers symbiotic nitrogen fixation and seed yield in soybean. Plant Biotechnology Journal, 20(1), 103-115. http://doi.org/10.1111/ pbi.13698. PMid:34487637.

Young, N. D., Debellé, F., Oldroyd, G. E., Geurts, R., Cannon, S. B., Udvardi, M. K., Benedito, V. A., Mayer, K. F., Gouzy, J., Schoof, H., Van de Peer, Y., Proost, S., Cook, D. R., Meyers, B. C., Spannagl, M., Cheung, F., De Mita, S., Krishnakumar, V., Gundlach, H., Zhou, S., Mudge, J., Bharti, A. K., Murray, J. D., Naoumkina, M. A., Rosen, B., Silverstein, K. A., Tang, H., Rombauts, S., Zhao, P. X., Zhou, P., Barbe, V., Bardou, P., Bechner, M., Bellec, A., Berger, A., Bergès, H., Bidwell, S., Bisseling, T., Choisne, N., Couloux, A., Denny, R., Deshpande, S., Dai, X., Doyle, J. J., Dudez, A. M., Farmer, A. D., Fouteau, S., Franken, C., Gibelin, C., Gish, J., Goldstein, S., González, A. J., Green, P. J., Hallab, A., Hartog, M., Hua, A., Humphray, S. J., Jeong, D. H., Jing, Y., Jöcker, A., Kenton, S. M., Kim, D. J., Klee, K., Lai, H., Lang, C., Lin, S., Macmil, S. L., Magdelenat, G., Matthews, L., McCorrison, J., Monaghan, E. L., Mun, J. H., Najar, F. Z., Nicholson, C., Noirot, C., O’Bleness, M., Paule, C. R., Poulain, J., Prion, F., Qin, B., Qu, C., Retzel, E. F., Riddle, C., Sallet, E., Samain, S., Samson, N., Sanders, I., Saurat, O., Scarpelli, C., Schiex, T., Segurens, B., Severin, A. J., Sherrier, D. J., Shi, R., Sims, S., Singer, S. R., Sinharoy, S., Sterck, L., Viollet, A., Wang, B. B., Wang, K., Wang, M., Wang, X., Warfsmann, J., Weissenbach, J., White, D. D., White, J. D., Wiley, G. B., Wincker, P., Xing, Y., Yang, L., Yao, Z., Ying, F., Zhai, J., Zhou, L., Zuber, A., Dénarié, J., Dixon, R. A., May, G. D., Schwartz, D. C., Rogers, J., Quétier, F., Town, C. D., & Roe, B. A. (2011). The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature, 480(7378), 520-524. http://doi.org/10.1038/nature10625. PMid: 22089132.

Yu, J., Tu, L., Subburaj, S., Bae, S., & Lee, G. J. (2021). Simultaneous targeting of duplicated genes in Petunia protoplasts for flower color modification via CRISPR-Cas9 ribonucleoproteins. Plant Cell Reports, 40(6), 1037-1045. http://doi.org/10.1007/s00299-020- 02593-1. PMid:32959126.

Yuan, M., Zhu, J., Gong, L., He, L., Lee, C., Han, S., Chen, C., & He, G. (2019). Mutagenesis of FAD2 genes in peanut with CRISPR/ Cas9 based gene editing. BMC Biotechnology, 19(1), 24. http:// doi.org/10.1186/s12896-019-0516-8. PMid:31035982.

Yue, J. J., Yuan, J. L., Wu, F. H., Yuan, Y. H., Cheng, Q. W., Hsu, C. T., & Lin, C. S. (2021). Protoplasts: From isolation to CRISPR/Cas genome editing application. Frontiers in Genome Editing, 3, 717017. http://doi.org/10.3389/fgeed.2021.717017. PMid:34713263.

Zafar, S. A., Zaidi, S. S. E. A., Gaba, Y., Singla-Pareek, S. L., Dhankher, O. P., Li, X., Mansoor, S., & Pareek, A. (2020). Engineering abiotic stress tolerance via CRISPR/Cas-mediated genome editing. Journal of Experimental Botany, 71(2), 470-479. http://doi.org/10.1093/ jxb/erz476. PMid:31644801.

Zander, P., Amjath-Babu, T. S., Preissel, S., Reckling, M., Bues, A., Schläfke, N., Kuhlman, T., Bachinger, J., Uthes, S., Stoddard, F., Murphy-Bokern, D., & Watson, C. (2016). Grain legume decline and potential recovery in European agriculture: A review. Agronomy for Sustainable Development, 36(2), 1-20. http://doi.org/10.1007/ s13593-016-0365-y.

Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., Essletzbichler, P., Volz, S. E., Joung, J., van der Oost, J., Regev, A., Koonin, E. V., & Zhang, F. (2015). Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163(3), 759-771. http://doi.org/10.1016/j.cell.2015.09.038. PMid:26422227.

Zhang, H., Cao, Y., Zhang, H., Xu, Y., Zhou, C., Liu, W., Zhu, R., Shang, C., Li, J., Shen, Z., Guo, S., Hu, Z., Fu, C., & Sun, D. (2020a). Efficient generation of CRISPR/Cas9-mediated homozygous/ biallelic Medicago truncatula mutants using a hairy root system. Frontiers in Plant Science, 11, 294. http://doi.org/10.3389/ fpls.2020.00294. PMid:32265954.

Zhang, Y., Wang, X., Luo, Y., Zhang, L., Yao, Y., Han, L., Che, Z., Wang, L., & Li, Y. (2020b). OsABA8ox2, an ABA catabolic gene, suppresses root elongation of rice seedlings and contributes to drought response. The Crop Journal, 8(3), 480-491. http://doi. org/10.1016/j.cj.2019.08.006.

Zhang, Y., Iaffaldano, B., & Qi, Y. (2021). CRISPR ribonucleoproteinmediated genetic engineering in plants. Plant Communications, 2(2), 100168. http://doi.org/10.1016/j.xplc.2021.100168. PMid:33898980.

Zhang, Y., Malzahn, A. A., Sretenovic, S., & Qi, Y. (2019). The emerging and uncultivated potential of CRISPR technology in plant science. Nature Plants, 5(8), 778-794. http://doi.org/10.1038/ s41477-019-0461-5. PMid:31308503.

Zheng, N., Li, T., Dittman, J. D., Su, J., Li, R., Gassmann, W., Peng, D., Whitham, S. A., Liu, S., & Yang, B. (2020). CRISPR/Cas9-based gene editing using egg cell-specific promoters in Arabidopsis and soybean. Frontiers in Plant Science, 11, 800. http://doi. org/10.3389/fpls.2020.00800. PMid:32612620.

Zhuang, W., Chen, H., Yang, M., Wang, J., Pandey, M. K., Zhang, C., Chang, W. C., Zhang, L., Zhang, X., Tang, R., Garg, V., Wang, X., Tang, H., Chow, C. N., Wang, J., Deng, Y., Wang, D., Khan, A. W., Yang, Q., Cai, T., Bajaj, P., Wu, K., Guo, B., Zhang, X., Li, J., Liang, F., Hu, J., Liao, B., Liu, S., Chitikineni, A., Yan, H., Zheng, Y., Shan, S., Liu, Q., Xie, D., Wang, Z., Khan, S. A., Ali, N., Zhao, C., Li, X., Luo, Z., Zhang, S., Zhuang, R., Peng, Z., Wang, S., Mamadou, G., Zhuang, Y., Zhao, Z., Yu, W., Xiong, F., Quan, W., Yuan, M., Li, Y., Zou, H., Xia, H., Zha, L., Fan, J., Yu, J., Xie, W., Yuan, J., Chen, K., Zhao, S., Chu, W., Chen, Y., Sun, P., Meng, F., Zhuo, T., Zhao, Y., Li, C., He, G., Zhao, Y., Wang, C., Kavikishor, P. B., Pan, R. L., Paterson, A. H., Wang, X., Ming, R., & Varshney, R. K. (2019). The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nature Genetics, 51(5), 865-876. http://doi. org/10.1038/s41588-019-0402-2. PMid:31043757.

Submitted date:
11/13/2023

Accepted date:
03/01/2024

Advancements and challenges in CRISPR/cas genome editing for legume crops

Tatiana Faria Maia; Joaquin Felipe Roca Paixão; Marcia Soares Vidal; Krzysztof Szczyglowski; Jean Luiz Simões de Araújo

Abstract

Keywords

References

Links

Share

BIORI