Journal of Innovative Agriculture, Volume 10, Issue 4 : 1-20. Doi : 10.37446/jinagri/ra/10.4.2023.1-20
Review Article

OPEN ACCESS | Published on : 31-Dec-2023

CRISPR-Cas9 mediated genome editing in soybean for improving quality traits

  • Ali Haider
  • Department of Plant Breeding and Genetics, Faculty of Agriculture, University of Agriculture Faisalabad, Faisalabad, Pakistan.
  • Umar Azam
  • Department of Plant Breeding and Genetics, Faculty of Agriculture, University of Agriculture Faisalabad, Faisalabad, Pakistan.
  • Amina Zia
  • Department of Microbiology, University Of Agriculture Faisalabad, Pakistan.
  • Aniqah Akhter
  • Department of Biotechnology, COMSAT University Islamabad, Islamabad, Pakistan.
  • Rabia Iqbal
  • Department of Home Sciences, University of Ari culture Faisalabad, Pakistan.
  • Rabia Naz
  • Department of National Institute of Food Science and Technology, Faculty of Food Nutrition and Home Sciences, University of Agriculture, Faisalabad, Pakistan.
  • Muhammad Atif
  • Department of Entomology, Faculty of Agriculture, University of Agriculture Faisalabad, Faisalabad, Pakistan.
  • Muhammad Fahad Iqbal
  • Department of Plant Breeding and Genetics, Faculty of Agriculture, University of Agriculture Faisalabad, Faisalabad, Pakistan.
  • Saima Majeed
  • Department of Botany, University of Agriculture Faisalabad, Faisalabad, Pakistan.
  • Ayesha Ashraf
  • Department of Plant Breeding and Genetics, Faculty of Agriculture, University of Agriculture Faisalabad, Faisalabad, Pakistan.

Abstract

Legumes are the major source of energy for people throughout the world and play a significant role in a balanced diet to satisfy the body's need for protein. Soybean (Glycine max L.) is also a poor man meat which is a highly enriched amount of protein present in it. Day-by-day increase in the worldwide population is also a great challenge to improve the yield and nutritional values. Here are some exciting ways to improve the yield and nutrition values through basic and advanced techniques that are particularly important and worldwide use. A unique idea called "biofortification" involves the enrichment of micronutrients using traditional plant breeding and contemporary technologies. Research on grain bio-fortification has considerably reduced hunger globally over the past few decades. The current bio-fortification programs are now more competitive due to a better understanding of the food matrix. Recent advancements in biotechnology have a variety of positive effects, and genetic engineering is developing quickly. Since genome editing technology has made it possible to precisely alter and change the genomes of living beings, it has transformed genetic and biological research, the simplest example is CRISPR CAS9. We concentrate on the most recent developments in CRISPR/Cas9-based technology and talk about the prospects and difficulties of using this ground-breaking technology to improve specific characteristics in soybeans and other crops.

Keywords

CRISPR CAS9, soybean, genome editing, quality traits, biofortification

References

  • 2021: A year marked by conflict, COVID and climate change | UNICEF. (n.d.). Retrieved April 5, 2023, from https://www.unicef.org/stories/2021-year-marked-conflict-covid-and-climate-change

    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), 1–10.

    Amirkhanov, R., & Stepanov, G. (2019). Systems of Delivery of CRISPR/Cas9 Ribonucleoprotein Complexes for Genome Editing. Russian Journal of Bioorganic Chemistry, 45, 431–437. https://doi.org/10.1134/S1068162019060025

    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.-S. P., & Cao, D. (2019). CRISPR/Cas9-mediated targeted mutagenesis of GmSPL9 genes alters plant architecture in soybean. BMC Plant Biology, 19(1), 131. https://doi.org/10.1186/s12870-019-1746-6

    Bao, A., Zhang, C., Huang, Y., Chen, H., Zhou, X., & Cao, D. (2020). Genome editing technology and application in soybean improvement. Oil Crop Science, 5(1), 31–40. https://doi.org/10.1016/j.ocsci.2020.03.001

    Bhagwat, A. C., Patil, A. M., & Saroj, S. D. (2022). CRISPR/Cas 9-based editing in the production of bioactive molecules. Molecular Biotechnology, 1–7.

    Budryn, G., Grzelczyk, J., & Pérez-Sánchez, H. (2018). Binding of red clover isoflavones to actin as a potential mechanism of anti-metastatic activity restricting the migration of cancer cells. Molecules, 23(10), 2471.

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

    Cai, Y., Chen, L., Sun, S., Wu, C., Yao, W., Jiang, B., Han, T., & Hou, W. (2018). CRISPR/Cas9-Mediated Deletion of Large Genomic Fragments in Soybean. International Journal of Molecular Sciences, 19(12), 3835. https://doi.org/10.3390/ijms19123835

    Cai, Y., Wang, L., Chen, L., Wu, T., Liu, L., Sun, S., Wu, C., Yao, W., Jiang, B., & Yuan, S. (2020). Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean. Plant Biotechnology Journal, 18(1), 298–309.

    Ceasar, S. A., Rajan, V., Prykhozhij, S. V., Berman, J. N., & Ignacimuthu, S. (2016). Insert, remove or replace: A highly advanced genome editing system using CRISPR/Cas9. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1863(9), 2333–2344.

    Chen, L., Nan, H., Kong, L., Yue, L., Yang, H., Zhao, Q., Fang, C., Li, H., Cheng, Q., & Lu, S. (2020). Soybean AP1 homologs control flowering time and plant height. Journal of Integrative Plant Biology, 62(12), 1868–1879.

    Cheng, Q., Dong, L., Su, T., Li, T., Gan, Z., Nan, H., Lu, S., Fang, C., Kong, L., & Li, H. (2019). CRISPR/Cas9-mediated targeted mutagenesis of GmLHY genes alters plant height and internode length in soybean. BMC Plant Biology, 19, 1–11.

    Chilcoat, D., Liu, Z.-B., & Sander, J. (2017). Chapter Two—Use of CRISPR/Cas9 for Crop Improvement in Maize and Soybean. In D. P. Weeks & B. Yang (Eds.), Progress in Molecular Biology and Translational Science (Vol. 149, pp. 27–46). Academic Press. https://doi.org/10.1016/bs.pmbts.2017.04.005

    Cicek, M. S., Chen, P., Saghai Maroof, M. A., & Buss, G. R. (2006). Interrelationships among agronomic and seed quality traits in an interspecific soybean recombinant inbred population. Crop Science, 46(3), 1253–1259.

    Coon, C. N., Leske, K. L., Akavanichan, O., & Cheng, T. K. (1990). Effect of oligosaccharide-free soybean meal on true metabolizable energy and fiber digestion in adult roosters. Poultry Science, 69(5), 787–793.

    Curtin, S. J., Zhang, F., Sander, J. D., Haun, W. J., Starker, C., Baltes, N. J., Reyon, D., Dahlborg, E. J., Goodwin, M. J., Coffman, A. P., Dobbs, D., Joung, J. K., Voytas, D. F., & Stupar, R. M. (2011). Targeted Mutagenesis of Duplicated Genes in Soybean with Zinc-Finger Nucleases. Plant Physiology, 156(2), 466–473. https://doi.org/10.1104/pp.111.172981

    Demorest, Z. L., Coffman, A., Baltes, N. J., Stoddard, T. J., Clasen, B. M., Luo, S., Retterath, A., Yabandith, A., Gamo, M. E., Bissen, J., Mathis, L., Voytas, D. F., & Zhang, F. (2016). Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biology, 16(1), 225. https://doi.org/10.1186/s12870-016-0906-1

    Do, P. T., Nguyen, C. X., Bui, H. T., Tran, L. T. N., Stacey, G., Gillman, J. D., Zhang, Z. J., & Stacey, M. G. (2019a). 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. https://doi.org/10.1186/s12870-019-1906-8

    Do, P. T., Nguyen, C. X., Bui, H. T., Tran, L. T., Stacey, G., Gillman, J. D., Zhang, Z. J., & Stacey, M. G. (2019b). 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, 1–14.

    Dong, O. X., Yu, S., Jain, R., Zhang, N., Duong, P. Q., Butler, C., Li, Y., Lipzen, A., Martin, J. A., Barry, K. W., Schmutz, J., Tian, L., & Ronald, P. C. (2020). Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nature Communications, 11(1), 1178. https://doi.org/10.1038/s41467-020-14981-y

    Doudna, J. A., & Charpentier, E. (2014). The new frontier of genome engineering with CRISPR-Cas9. Science, 346(6213), 1258096.

    Du, H., Zeng, X., Zhao, M., Cui, X., Wang, Q., Yang, H., Cheng, H., & Yu, D. (2016). Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. Journal of Biotechnology, 217, 90–97.

    Elvira-Torales, L. I., García-Alonso, J., & Periago-Castón, M. J. (2019). Nutritional importance of carotenoids and their effect on liver health: A review. Antioxidants, 8(7), 229.

    First Commercial Sale of Calyxt High Oleic Soybean Oil on the U.S. Market | AP News. (n.d.). Retrieved April 5, 2023, from https://apnews.com/article/business-lifestyle-health-minneapolis-agriculture-d4d2190346a14d639bb629902f487883

    Flavor problems of vegetable food proteins—Rackis—1979—Journal of the American Oil Chemists’ Society—Wiley Online Library. (n.d.). Retrieved June 27, 2023, from https://aocs.onlinelibrary.wiley.com/doi/abs/10.1007/BF02671470?casa_token=TOMCVvzkCIkAAAAA:yWRS6bmyS9ykJGpMVqSs2FH3O9vvCNnyocGV4UgqKQECVRmvHbtZepmoRZIdMgwTTX55HrAXLnfRc82L

    Frassinetti, S., Bronzetti, G., Caltavuturo, L., Cini, M., & Croce, C. D. (2006). The role of zinc in life: A review. Journal of Environmental Pathology, Toxicology and Oncology: Official Organ of the International Society for Environmental Toxicology and Cancer, 25(3), 597–610. https://doi.org/10.1615/jenvironpatholtoxicoloncol.v25.i3.40

    Gratz, S. J., Cummings, A. M., Nguyen, J. N., Hamm, D. C., Donohue, L. K., Harrison, M. M., Wildonger, J., & O’Connor-Giles, K. M. (2013). Genome Engineering of Drosophila with the CRISPR RNA-Guided Cas9 Nuclease. Genetics, 194(4), 1029–1035. https://doi.org/10.1534/genetics.113.152710

    Herman, E. M., Helm, R. M., Jung, R., & Kinney, A. J. (2003). Genetic Modification Removes an Immunodominant Allergen from Soybean,. Plant Physiology, 132(1), 36–43. https://doi.org/10.1104/pp.103.021865

    Hill, J. H., & Whitham, S. A. (2014). Control of virus diseases in soybeans. In Advances in virus research (Vol. 90, pp. 355–390). Elsevier.

    Hou, A., Chen, P., Shi, A., Zhang, B., & Wang, Y.-J. (2009). Sugar variation in soybean seed assessed with a rapid extraction and quantification method. International Journal of Agronomy, 2009.

    Hsu, P. D., Lander, E. S., & Zhang, F. (2014). Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157(6), 1262–1278.

    Hua, K., Zhang, J., Botella, J. R., Ma, C., Kong, F., Liu, B., & Zhu, J.-K. (2019). Perspectives on the Application of Genome-Editing Technologies in Crop Breeding. Molecular Plant, 12(8), 1047–1059. https://doi.org/10.1016/j.molp.2019.06.009

    Hwang, S., & Lee, T. G. (2019). Integration of lodging resistance QTL in soybean. Scientific Reports, 9(1), 6540. https://doi.org/10.1038/s41598-019-42965-6

    Hyten, D. L., Song, Q., Zhu, Y., Choi, I.-Y., Nelson, R. L., Costa, J. M., Specht, J. E., Shoemaker, R. C., & Cregan, P. B. (2006). Impacts of genetic bottlenecks on soybean genome diversity. Proceedings of the National Academy of Sciences, 103(45), 16666–16671. https://doi.org/10.1073/pnas.0604379103

    Ibrahim, S., Saleem, B., Rehman, N., Zafar, S. A., Naeem, M. K., & Khan, M. R. (2022). CRISPR/Cas9 mediated disruption of Inositol Pentakisphosphate 2-Kinase 1 (TaIPK1) reduces phytic acid and improves iron and zinc accumulation in wheat grains. Journal of Advanced Research, 37, 33–41. https://doi.org/10.1016/j.jare.2021.07.006

    Imaizumi, T., & Kay, S. A. (2006). Photoperiodic control of flowering: Not only by coincidence. Trends in Plant Science, 11(11), 550–558.

    Jacobs, T. B., LaFayette, P. R., Schmitz, R. J., & Parrott, W. A. (2015a). Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnology, 15(1), 16. https://doi.org/10.1186/s12896-015-0131-2

    Jacobs, T. B., LaFayette, P. R., Schmitz, R. J., & Parrott, W. A. (2015b). Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnology, 15, 1–10.

    Jain, M. (2015). Function genomics of abiotic stress tolerance in plants: A CRISPR approach. In Frontiers in plant science (Vol. 6, p. 375). Frontiers Media SA.

    Jimenez, K., Kulnigg-Dabsch, S., & Gasche, C. (2015). Management of Iron Deficiency Anemia. Gastroenterology & Hepatology, 11(4), 241–250.

    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. https://doi.org/10.1126/science.1225829

    Kara, S. R., Choudhuryb, S., & Chakrabortyc, A. (n.d.). CRISPR/Cas9 for soybean improvement: A review.

    Kennedy, I. R., Mwandemele, O. D., & McWhirter, K. S. (1985). Estimation of sucrose, raffinose and stachyose in soybean seeds. Food Chemistry, 17(2), 85–93.

    Kumar, D., Yadav, A., Ahmad, R., Dwivedi, U. N., & Yadav, K. (2022). CRISPR-Based Genome Editing for Nutrient Enrichment in Crops: A Promising Approach Toward Global Food Security. Frontiers in Genetics, 13. https://www.frontiersin.org/articles/10.3389/fgene.2022.932859

    Kumssa, D. B., Joy, E. J. M., Ander, E. L., Watts, M. J., Young, S. D., Walker, S., & Broadley, M. R. (2015). Dietary calcium and zinc deficiency risks are decreasing but remain prevalent. Scientific Reports, 5, 10974. https://doi.org/10.1038/srep10974

    Le, H., Nguyen, N. H., Ta, D. T., Le, T. N. T., Bui, T. P., Le, N. T., Nguyen, C. X., Rolletschek, H., Stacey, G., & Stacey, M. G. (2020). CRISPR/Cas9-mediated knockout of galactinol synthase-encoding genes reduces raffinose family oligosaccharide levels in soybean seeds. Frontiers in Plant Science, 2033.

    Le, H., Nguyen, N. H., Ta, D. T., Le, T. N. T., Bui, T. P., Le, N. T., Nguyen, C. X., Rolletschek, H., Stacey, G., Stacey, M. G., Pham, N. B., Do, P. T., & Chu, H. H. (2020). CRISPR/Cas9-Mediated Knockout of Galactinol Synthase-Encoding Genes Reduces Raffinose Family Oligosaccharide Levels in Soybean Seeds. Frontiers in Plant Science, 11, 612942. https://doi.org/10.3389/fpls.2020.612942

    Li, M., Liu, Y., Wang, C., Yang, X., Li, D., Zhang, X., Xu, C., Zhang, Y., Li, W., & Zhao, L. (2020). Identification of Traits Contributing to High and Stable Yields in Different Soybean Varieties Across Three Chinese Latitudes. Frontiers in Plant Science, 10. https://www.frontiersin.org/articles/10.3389/fpls.2019.01642

    Li, T., Liu, B., Spalding, M. H., Weeks, D. P., & Yang, B. (2012). High-efficiency TALEN-based gene editing produces disease-resistant rice. Nature Biotechnology, 30(5), Article 5. https://doi.org/10.1038/nbt.2199

    Li, Z., Moon, B. P., Xing, A., Liu, Z.-B., McCardell, R. P., Damude, H. G., & Falco, S. C. (2010). Stacking multiple transgenes at a selected genomic site via repeated recombinase-mediated DNA cassette exchanges. Plant Physiology, 154(2), 622–631.

    Liu, J., Gunapati, S., Mihelich, N. T., Stec, A. O., Michno, J.-M., & Stupar, R. M. (2019). Genome Editing in Soybean with CRISPR/Cas9. In Y. Qi (Ed.), Plant Genome Editing with CRISPR Systems: Methods and Protocols (pp. 217–234). Springer. https://doi.org/10.1007/978-1-4939-8991-1_16

    Liu, M., Rehman, S., Tang, X., Gu, K., Fan, Q., Chen, D., & Ma, W. (2019). Methodologies for improving HDR efficiency. Frontiers in Genetics, 9, 691.

    Liu, R., Hu, Y., Li, J., & Lin, Z. (2007). Production of soybean isoflavone genistein in non-legume plants via genetically modified secondary metabolism pathway. Metabolic Engineering, 9(1), 1–7. https://doi.org/10.1016/j.ymben.2006.08.003

    Liu, Z., Dong, H., Cui, Y., Cong, L., & Zhang, D. (2020). Application of different types of CRISPR/Cas-based systems in bacteria. Microbial Cell Factories, 19(1), 1–14.

    Lu, C., Napier, J. A., Clemente, T. E., & Cahoon, E. B. (2011). New frontiers in oilseed biotechnology: Meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications. Current Opinion in Biotechnology, 22(2), 252–259.

    Ma, J., Sun, S., Whelan, J., & Shou, H. (2021a). CRISPR/Cas9-mediated knockout of GmFATB1 significantly reduced the amount of saturated fatty acids in soybean seeds. International Journal of Molecular Sciences, 22(8), Article 8.

    Ma, J., Sun, S., Whelan, J., & Shou, H. (2021b). CRISPR/Cas9-mediated knockout of GmFATB1 significantly reduced the amount of saturated fatty acids in soybean seeds. International Journal of Molecular Sciences, 22(8), 3877.

    Malloy, K. M., Wang, J., Clark, L. H., Fang, Z., Sun, W., Yin, Y., Kong, W., Zhou, C., & Bae-Jump, V. L. (2018). Novasoy and genistein inhibit endometrial cancer cell proliferation through disruption of the AKT/mTOR and MAPK signaling pathways. American Journal of Translational Research, 10(3), 784.

    Maoka, T. (2020). Carotenoids as natural functional pigments. Journal of Natural Medicines, 74(1), 1–16. https://doi.org/10.1007/s11418-019-01364-x

    Marx, V. (2018). Base editing a CRISPR way. Nature Methods, 15(10), 767–770. https://doi.org/10.1038/s41592-018-0146-4

    Mellor, N., Bligh, F., Chandler, I., & Hodgman, C. (2010). Reduction of Off-Flavor Generation in Soybean Homogenates: A Mathematical Model. Journal of Food Science, 75(7), R131–R138.

    Mladenov, E., & Iliakis, G. (2011). Induction and repair of DNA double strand breaks: The increasing spectrum of non-homologous end joining pathways. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 711(1–2), 61–72. https://doi.org/10.1016/j.mrfmmm.2011.02.005

    Myoung Hui Lee, Jiyoung Lee, Seung A Choi, Ye-Sol Kim, Okjae Koo, Seung Hee Choi, Woo Seok Ahn, Eun Yee Jie, & Suk Weon Kim. (2020). Efficient genome editing using CRISPR–Cas9 RNP delivery into cabbage protoplasts via electro-transfection. Plant Biotechnology Reports, 14(6), 695–702. https://doi.org/10.1007/s11816-020-00645-2

    Naveed, M., Javed, J., Waheed, U., Sajid, M., Ijaz, M., Sehar, A., Attique, M., & Javed, S. (2022). The Role of CRISPR/Cas9 for Genetic Advancement of Soybean: A Review. Asian Journal of Biotechnology and Genetic Engineering, 5(4), 75–88.

    Nielsen, N. C., Dickinson, C. D., Cho, T.-J., Thanh, V. H., Scallon, B. J., Fischer, R. L., Sims, T. L., Drews, G. N., & Goldberg, R. B. (1989). Characterization of the glycinin gene family in soybean. The Plant Cell, 1(3), 313–328.

    Oerke, E.-C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144(1), 31–43.

    Patil, G., Vuong, T. D., Kale, S., Valliyodan, B., Deshmukh, R., Zhu, C., Wu, X., Bai, Y., Yungbluth, D., & Lu, F. (2018). Dissecting genomic hotspots underlying seed protein, oil, and sucrose content in an interspecific mapping population of soybean using high-density linkage mapping. Plant Biotechnology Journal, 16(11), 1939–1953.

    Ricroch, A., Clairand, P., & Harwood, W. (2017a). Use of CRISPR systems in plant genome editing: Toward new opportunities in agriculture. Emerging Topics in Life Sciences, 1(2), 169–182.

    Ricroch, A., Clairand, P., & Harwood, W. (2017b). Use of CRISPR systems in plant genome editing: Toward new opportunities in agriculture. Emerging Topics in Life Sciences, 1(2), 169–182. https://doi.org/10.1042/ETLS20170085

    Sathyapalan, T., Aye, M., Rigby, A. S., Thatcher, N. J., Dargham, S. R., Kilpatrick, E. S., & Atkin, S. L. (2018). Soy isoflavones improve cardiovascular disease risk markers in women during the early menopause. Nutrition, Metabolism and Cardiovascular Diseases, 28(7), 691–697.

    Schaeffer, S. M., & Nakata, P. A. (2015). CRISPR/Cas9-mediated genome editing and gene replacement in plants: Transitioning from lab to field. Plant Science, 240, 130–142. https://doi.org/10.1016/j.plantsci.2015.09.011

    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., … Jackson, S. A. (2010). Genome sequence of the palaeopolyploid soybean. Nature, 463(7278), Article 7278. https://doi.org/10.1038/nature08670

    Schuler, M. A., Ladin, B. F., Pollaco, J. C., Freyer, G., & Beachy, R. N. (1982). Structural sequences are conserved in the genes coding for the α, α′ and β-subunits of the soybean 7S seed storage protein. Nucleic Acids Research, 10(24), 8245–8261.

    Sebastian, S. A., Fader, G. M., Ulrich, J. F., Forney, D. R., & Chaleff, R. S. (1989). Semidominant soybean mutation for resistance to sulfonylurea herbicides. Crop Science, 29(6), 1403–1408.

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

    Siddique, S. (2022a). Role of CRISPR/Cas9 in Soybean (Glycine max L.) Quality Improvement. In Soybean—Recent Advances in Research and Applications. IntechOpen. https://doi.org/10.5772/intechopen.102812

    Siddique, S. (2022b). Role of CRISPR/Cas9 in Soybean (Glycine max L.) Quality Improvement. In Soybean—Recent Advances in Research and Applications. IntechOpen. https://doi.org/10.5772/intechopen.102812

    Singh, R. J. (2017). Botany and Cytogenetics of Soybean. In H. T. Nguyen & M. K. Bhattacharyya (Eds.), The Soybean Genome (pp. 11–40). Springer International Publishing. https://doi.org/10.1007/978-3-319-64198-0_2

    Sinha, P., Davis, J., Saag, L., Wanke, C., Salgame, P., Mesick, J., Horsburgh, C. R., & Hochberg, N. S. (2019). Undernutrition and Tuberculosis: Public Health Implications. The Journal of Infectious Diseases, 219(9), 1356–1363. https://doi.org/10.1093/infdis/jiy675

    Sommer, A. (2008). Vitamin a deficiency and clinical disease: An historical overview. The Journal of Nutrition, 138(10), 1835–1839. https://doi.org/10.1093/jn/138.10.1835

    Sugano, S., Hirose, A., Kanazashi, Y., Adachi, K., Hibara, M., Itoh, T., Mikami, M., Endo, M., Hirose, S., & Maruyama, N. (2020). Simultaneous induction of mutant alleles of two allergenic genes in soybean by using site-directed mutagenesis. BMC Plant Biology, 20(1), 1–15.

    Sun, L., Miao, Z., Cai, C., Zhang, D., Zhao, M., Wu, Y., Zhang, X., Swarm, S. A., Zhou, L., Zhang, Z. J., Nelson, R. L., & Ma, J. (2015). GmHs1-1, encoding a calcineurin-like protein, controls hard-seededness in soybean. Nature Genetics, 47(8), 939–943. https://doi.org/10.1038/ng.3339

    Sun, S.-K., Xu, X., Tang, Z., Tang, Z., Huang, X.-Y., Wirtz, M., Hell, R., & Zhao, F.-J. (2021). A molecular switch in sulfur metabolism to reduce arsenic and enrich selenium in rice grain. Nature Communications, 12(1), 1392. https://doi.org/10.1038/s41467-021-21282-5

    Sun, Y., Zhang, X., Wu, C., He, Y., Ma, Y., Hou, H., Guo, X., Du, W., Zhao, Y., & Xia, L. (2016). Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Molecular Plant, 9(4), 628–631.

    Sun, Z., Su, C., Yun, J., Jiang, Q., Wang, L., Wang, Y., Cao, D., Zhao, F., Zhao, Q., & Zhang, M. (2019). Genetic improvement of the shoot architecture and yield in soya bean plants via the manipulation of GmmiR156b. Plant Biotechnology Journal, 17(1), 50–62.

    Two soybean seed lipoxygenase nulls accumulate reduced levels of lipoxygenase transcripts | SpringerLink. (n.d.). Retrieved June 27, 2023, from https://link.springer.com/article/10.1007/BF00020127

    Wang, J., Kuang, H., Zhang, Z., Yang, Y., Yan, L., Zhang, M., Song, S., & Guan, Y. (2020). Generation of seed lipoxygenase-free soybean using CRISPR-Cas9. The Crop Journal, 8(3), 432–439.

    Wang, S., Yokosho, K., Guo, R., Whelan, J., Ruan, Y.-L., Ma, J. F., & Shou, H. (2019). The soybean sugar transporter GmSWEET15 mediates sucrose export from endosperm to early embryo. Plant Physiology, 180(4), 2133–2141.

    Wu, N., Lu, Q., Wang, P., Zhang, Q., Zhang, J., Qu, J., & Wang, N. (2020). Construction and analysis of GmFAD2-1A and GmFAD2-2A soybean fatty acid desaturase mutants based on CRISPR/Cas9 technology. International Journal of Molecular Sciences, 21(3), 1104.

    Xu, H., Zhang, L., Zhang, K., & Ran, Y. (2020). Progresses, Challenges, and Prospects of Genome Editing in Soybean (Glycine max). Frontiers in Plant Science, 11. https://www.frontiersin.org/articles/10.3389/fpls.2020.571138

    Yang, X., Li, X., Shan, J., Li, Y., Zhang, Y., Wang, Y., Li, W., & Zhao, L. (2021). Overexpression of GmGAMYB accelerates the transition to flowering and increases plant height in soybean. Frontiers in Plant Science, 12, 667242.

    Zhang, P., Du, H., Wang, J., Pu, Y., Yang, C., Yan, R., Yang, H., Cheng, H., & Yu, D. (2020). Multiplex CRISPR/Cas9-mediated metabolic engineering increases soya bean isoflavone content and resistance to soya bean mosaic virus. Plant Biotechnology Journal, 18(6), 1384–1395. https://doi.org/10.1111/pbi.13302

    Zhang, Y., Zhang, F., Li, X., Baller, J. A., Qi, Y., Starker, C. G., Bogdanove, A. J., & Voytas, D. F. (2013). Transcription Activator-Like Effector Nucleases Enable Efficient Plant Genome Engineering. Plant Physiology, 161(1), 20–27. https://doi.org/10.1104/pp.112.205179

    Zhu, Y., Wu, N., Song, W., Yin, G., Qin, Y., Yan, Y., & Hu, Y. (2014). Soybean (Glycine max) expansin gene superfamily origins: Segmental and tandem duplication events followed by divergent selection among subfamilies. BMC Plant Biology, 14(1), 93. https://doi.org/10.1186/1471-2229-14-93