Rice grain yield and quality improvement via CRISPR/Cas9 system: an updated review


  • Aqib ZEB State Key Laboratory of Rice Biology/Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture/China National Rice Improvement Centre/China National Rice Research Institute, Hangzhou 310006 (CN)
  • Shakeel AHMAD University of Agriculture Faisalabad, National Center for Genome Editing for Crop Improvement and Human Health, Centre for Advanced Studies in Agriculture and Food Security, 38000 (PK)
  • Javaria TABBASUM University of the Punjab, Faculty of Agricultural Sciences, Department of Plant Breeding and Genetics, 54590 (CN)
  • Zhonghua SHENG State Key Laboratory of Rice Biology/Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture/China National Rice Improvement Centre/China National Rice Research Institute, Hangzhou 310006 (CN)
  • Peisong HU State Key Laboratory of Rice Biology/Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture/China National Rice Improvement Centre/China National Rice Research Institute, Hangzhou 310006 (CN)




base editing, CRISPR/Cas-9, genome editing, grain quality improvement, mega-nucleases, transgene free


Rice (Oryza sativa L.) is an important staple food crop worldwide. To meet the growing nutritional requirements of the increasing population in the face of climate change, qualitative and quantitative traits of rice need to be improved. During recent years, genome editing has played a great role in the development of superior varieties of grain crops. Genome editing and speed breeding have improved the accuracy and pace of rice breeding. New breeding technologies including genome editing have been established in rice, expanding the potential for crop improvement. Over a decade, site-directed mutagenesis tools like Zinc Finger Nucleases (ZFN), Transcriptional activator-like Effector Nucleases (TALENs), and Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) System were used and have played a great role in rice yield and quality enhancement. In addition, most recently other genome editing techniques like prime editing and base editors have also been used for efficient genome editing in rice. Since rice is an excellent model system for functional studies due to its small genome and close synthetic relationships with other cereal crops, new genome-editing technologies continue to be developed for use in rice. Genomic alteration employing genome editing technologies (GETs) like CRISPR/Cas9 for reverse genetics has opened new avenues in agricultural sciences such as rice yield and grain quality improvement. Currently, CRISPR/Cas9 technology is widely used by researchers for genome editing to achieve the desired biological objectives, because of its simple targeting, easy-to-design, cost-effective, and versatile tool for precise and efficient plant genome editing. Over the past few years many genes related to rice grain quality and yield enhancement have been successfully edited via CRISPR/Cas9 technology method to cater to the growing demand for food worldwide. The effectiveness of these methods is being verified by the researchers and crop scientists worldwide. In this review we focus on genome-editing tools for rice improvement to address the progress made and provide examples of genome editing in rice. We also discuss safety concerns and methods for obtaining transgene-free crops.


Metrics Loading ...


Abdelrahman M, Zhao K (2020). Genome editing and rice grain quality. The Future of Rice Demand: Quality Beyond Productivity. Springer, pp 395-422.

Abe K, Araki E, Suzuki Y, Toki S, Saika H (2018). Production of higholeic/low linoleic rice by genome editing. Plant Physiology and Biochemistry 131:58-62. https://doi.org/10.1016/j.plaphy.2018.04.033

Ahmad S, Tang L, Shahzad R, Mawia AM, Rao GS, Jamil S, ... Tang S (2021). CRISPR-based crop improvements: A way forward to achieve zero hunger. Journal of Agricultural and Food Chemistry 69(30):8307-8323. https://doi.org/10.1021/acs.jafc.1c02653

Ahmad S, Shahzad R, Jamil S, Tabassum J, Chaudhary MAM, Atif RM, ... Tang S (2021). Regulatory aspects, risk assessment, and toxicity associated with RNAi and CRISPR methods. In: CRISPR and RNAi Systems. pp 687-721, Elsevier. https://doi.org/10.1016/B978-0-12-821910-2.00013-8

Ahmar S, Gill RA, Jung KH, Faheem Am Qasim MU, Mubeen M, Zhou W (2020). Conventional and molecular techniques from simple breeding to speed breeding in crop plants: Recent advances and future outlook. International Journal of Molecular Sciences 21(7):2590. https://doi.org/10.3390/ijms21072590

Ain QU, Chung JY, Kim YH (2015). Current and future delivery systems for engineered nucleases: ZFN, TALEN and RGEN. Journal of Controlled Release 205:120-127. https://doi.org/10.1016/j.jconrel.2014.12.036

Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen P, Wilson C, Newby GA, Raguram A (2019). Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149-157. https://doi.org/10.1038/s41586-019-1711-4

Ansari A, Wang C, Wang J, Wang F, Liu P, Gao Y (2017). Engineered dwarf male-sterile rice: a promising genetic tool for facilitatingrecurrent selection in rice. Frontiers in Plant Science 8:2132. https://doi.org/10.3389/fpls.2017.02132

Ali Z, Abul-Faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, ... Mahfouz MM (2015). Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Molecular Plant 8:1288-1291. https://doi.org/10.1016/j.molp.2015.02.011

Azizi P, Osman M, Hanafi M, Sahebi M, Rafii M, Taheri S, . . . Yusuf M (2019). Molecular insights into the regulation of rice kernel elongation. Critical Reviews in Biotechnology 39(7):904-923. https://doi.org/10.1080/07388551.2019.1632257

Banakar R, Schubert M, Collingwood M, Vakulskas C, Eggenberger AL, Wang K (2020). Comparison of CRISPR-Cas9/Cas12a ribonucleoprotein complexes for genome editing efficiency in the rice phytoene desaturase (OsPDS) gene. Rice 13(1):1-7. https://doi.org/10.1186/s12284-019-0365-z

Birla DS, Malik K, Sainger M, Chaudhary D, Jaiwal R, Jaiwal PK (2017). Progress and challenges in improving the nutritional quality of rice (Oryza sativa L.). Critical Reviews in Food Science and Nutrition 57(11):2455-2481. https://doi.org/10.1080/10408398.2015.1084992

Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509-1512. https://doi.org.10.1126/science.1178811

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

Butt H, Eid A, Ali Z, Atia MA, Mokhtar MM, Hassan N, … Mahfouz MM (2017). Efficient CRISPR/Cas9-mediated genome editing using a chimericsingle-guide RNA molecule. Frontiers in Plant Science 8:1441. https://doi.org/10.3389/fpls.2017.01441

Butt H, Zaidi SSA, Hassan N, Mahfouz M (2020). CRISPR-based directed evolution for crop improvement. Trends in Biotechnology 38:236-240. https://doi.org/10.1016/j.tibtech.2019.08.001

Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR associated9 system. Plant Physiology 166:1292-1297. https://doi.org/10.1104/pp.114.247577

Chen X, Lu X, Shu N, Wang S, Wang J, Wang D, Guo L, Ye W (2017). Targeted mutagenesis in cotton Gossypium hirsutum L. using the CRISPR/Cas9 system. Scientific Reports 7:44304. https://doi.org/10.1038/srep44304

Calingacion M, Laborte A, Nelson A, Resurreccion A, Concepcion JC, Daygon VD, . . . Bassinello PZ (2014). Diversity of global rice markets and the science required for consumer-targeted rice breeding. PloS One 9(1):e85106. https://doi.org/10.1371/journal.pone.0085106

Cassandri M, Smirnov A, Novelli F, Pitolli C, Agostini M, Malewicz M, . . . Raschellà G (2017). Zinc-finger proteins in health and disease. Cell Death Discovery 3(1):17071. https://doi.org/10.1038/cddiscovery.2017.71

Clemens S, Aarts MG, Thomine S, Verbruggen N (2013). Plant science: the key to preventing slow cadmium poisoning. Trends in Plant Science 18:92-99. https://doi.org/10.1016/j.tplants.2012.08.003

Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Zhang F (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823. https://doi.org/10.1126/science.1231143

Cui Y, Hu X, Liang G, Feng A, Wang F, Ruan S, . . . Chen D (2020). Production of novel beneficial alleles of a rice yield‐related QTL by CRISPR/Cas9. Plant Biotechnology Journal 18(10):1987. https://doi.org/10.1111/pbi.13370

Chen Yu, Zhu A, Xue P, Wen X, Cao Y, Wang B, Shah L, Chang S, Zhang Y (2020). Effects of GS3 and GL3.1 for grain size editing by CRISPR/Cas 9 in rice. Rice Science 27(5):405-413. https://doi.org/10.1016/j.rsci.2019.12.010

Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S (2005). Zinc finger nucleases: Custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Research 33:5978-5990. https://doi.org/10.1093/nar/gki912

Endo A, Saika H, Takemura M, Misawa N, Toki S (2019). Anovel approach to carotenoid accumulation in rice callus by mimickingthe cauliflower orange mutation via genome editing. Rice 12:1-5. https://doi.org/10.1186/s12284-019-0345-3

Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, … Zhu JK (2014). Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences 111(12):4632-4637. https://doi.org/10.1073/pnas.1400822111

Gaj T, Gersbach CA, Barbas III CF (2013). ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology 31(7):397-405.%20https:/doi.org/10.1016/j.tibtech.2013.04.004

Gao X, Chen J, Dai X, Zhang D, Zhao Y (2016). An effective strategyfor reliably isolating heritable and Cas9-free arabidopsis mutants generatedby CRISPR/Cas9-mediated genome editing. Plant Physiology 171:1794-1800. https://doi.org/10.1104/pp.16.00663

Gao F, Shen XZ, Jiang F, Wu Y, Han C (2016). DNA-guided genome editing using the Natronobacterium gregoryi Argonaute. Nature Biotechnology 34:768-773. https:/doi.org/10.1038/nbt.3547.

Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012). Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proceedings of the National Academy of Sciences 109(39):E2579-E2586. https://doi.org/10.1073/pnas.1208507109

Hua K, Tao X, Zhu JK (2019). Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnology Journal 17(2):499-504. https://doi.org/10.1111/pbi.12993

Hamada H, Liu Y, Nagira Y, Miki R, Taoka N, Imai R (2018). Biolisticdelivery-based transient CRISPR/Cas9 expression enables in planta genomeediting in wheat. Scientific Reports 8:14422. https://doi.org/10.1038/s41598-018-32714-6

Huang L, Zhang R, Huang G, Li Y, Melaku G, Zhang S, . . . Zhang Y (2018). Developing superior alleles of yield genes in rice by artificial mutagenesis using the CRISPR/Cas9 system. The Crop Journal 6(5):475-481. https://doi.org/10.1016/j.cj.2018.05.005

Hui S, Li H, Mawia AM, Zhou L, Cai J, Ahmad S ... Hu P (2021). Production of aromatic three‐line hybrid rice using novel alleles of BADH2. Plant Biotechnology Journal 20(1):59-74. https://doi.org/10.1111/pbi.13695

Iaffaldano B, Zhang Y, Cornish K (2016). CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Industrial Crops and Products 89:356-362. https://doi.org/10.1016/j.indcrop.2016.05.029

Jena KK, Kim S-R (2020). Genomics, biotechnology and plant breeding for the improvement of rice production. In: Accelerated Plant Breeding. Springer, Volume 1, pp 217-232.

Jia H, Zhang Y, Orbovic V, Xu J, White F, Jones J, Wang N (2017). Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnology Journal 15:817-823. https://doi.org/10.1111/pbi.12677

Jia H, Wang N (2014). Targeted genome editing of sweet orange using Cas9/sgRNA. PloS One 9:e93806. https://doi.org/10.1371/journal.pone.0093806

Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013). Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research 41(20):e188-e188. https://doi.org/10.1093/nar/gkt780

Jiang H, Lio J, Blanco M, Campbell M, Jane J-l (2010). Resistant-starch formation in high-amylose maize starch during kernel development. Journal of Agricultural and Food Chemistry 58:8043-8047. https:/doi.org/10.1021/jf101056y

Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, . . . Li J (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics 42:541-544. https://doi.org/10.1038/ng.591

Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, 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

Jung YJ, Lee HJ, Bae S, Kim JH, Kim DH, Kim HK, … Kang KK (2019). Acquisition of seed dormancy breaking in rice (Oryza sativa L.) via CRISPR/Cas9-targeted mutagenesis of OsVP1 gene. Plant Biotechnology Reports 13:511-520. https://doi.org/10.1007/s11816-019-00580-x

Kamburova VS, Nikitina EV, Shermatov SE, Buriev ZT, Kumpatla SP, Emani C, Abdurakhmonov IY (2017). Genome editing in plants: an overview of tools and applications. International Journal of Agronomy 7315351. https://doi.org/10.1155/2017/7315351

Kim H, Kim JS (2014). A guide to genome engineering with programmable nucleases. Nature Reviews Genetics 15:321-334. https://doi.org/10.1038/nrg3686

Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT, Liu DR (2017). Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nature Biotechnology 35:371-376. https://doi.org.10.1038/nbt.3803.

Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V (2019). A male expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565:91-95. https://doi.org.10.1038/s41586-018-0785-8

Khan Z, Khan SH, Mubarik MS, Sadia B, Ahmad A (2017). Use of TALEs and TALEN technology for genetic improvement of plants. Plant Molecular Biology Reporter 35(1):1-19. https://doi.org/10.1007/s11105-016-0997-8

Khush GS (2005). What it will take to feed 5.0 billion rice consumers in 2030. Plant Molecular Biology 59(1):1-6. https://doi.org/10.1007/s11103-005-2159-5

Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016). Programmable editing of target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420-424. https://doi.org/10.1038/nature17946

Kohli A, Miro B, Balié J, d’A Hughes J (2020). Photosynthesis research: a model to bridge fundamental science, translational products, and socio-economic considerations in agriculture. Journal of Experimental Botany 71(7):2281-2298. https://doi.org/10.1093/jxb/eraa087

Kopischke S, Schüßler E, Althoff F, Zachgo S (2017). TALEN-mediated genome-editing approaches in the liverwort Marchantia polymorpha yield high efficiencies for targeted mutagenesis. Plant Methods 13:20. https://doi.org/10.1186/s13007-017-0167-5

Kuang Y, Li S, Ren B, Yan F, Spetz C, Li X, . . . Zhou H (2020). Base-editing-mediated artificial evolution of OsALS1 in planta to develop novel herbicide-tolerant rice germplasms. Molecular Plants 13. https://doi.org/10.1016/j.molp.2020.01.010

Lacchini E, Kiegle E, Castellani M, Adam H, Jouannic S, Gregis V, Kater MM (2020). CRISPR-mediated accelerated domestication of African rice landraces. PloS One 15(3):e0229782. https://doi.org/10.1371/journal.pone.0229782

Li ZK, Chen B, Li XX, Wang JP, Zhang Y, Wang XF, ... Ma ZY (2019). A newly identified cluster of glutathione S‐transferase genes provides Verticillium wilt resistance in cotton. The Plant Journal 98(2):213-227. https://doi.org/10.1111/tpj.14206

Li C, Zhang R, Meng X, Chen S, Zong Y, Lu C, ... Gao C (2020). Targeted,random mutagenesis of plant genes with dual cytosine and adenine base editors. Nature Biotechnology 38:875-882. https://doi.org/10.1038/s41587-019-0393-7

Li H, Li J, Chen J, Yan L, Xia L (2020). Precise modifications of both exogenous and endogenous genes in rice by prime editing. Molecular Plant 13(5):671-674. https://doi.org/10.1016/j.molp.2020.03.011

Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, . . . Gao C (2016). Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nature Plants 2:16139. https://doi.org/10.1038/nplants.2016.139

Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM (2015). Cas9-guide RNA directed genome editing in soybean. Plant Physiology 169:960-970. https://doi.org/10.1104/pp.15.00783

Li S, Zhao B, Yuan D, Duan M, Qian Q, Tang L, . . . Li C (2013). Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proceedings of the National Academy of Sciences 110(8):3167-3172. https://doi.org/10.1073/pnas.1300359110

Li JF, Norville JE, Aach J, Mccormack M, Zhang D, Bush J, Church GM, Sheen J (2013). Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology 31:688. https://doi.org/10.1038/nbt.2654

Li Y, Fan C, Xing Y, Yun P, Luo L, Yan B, . . . He Y (2014). Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nature Genetics 46:398-404. https://doi.org/10.1038/ng.2923

Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012). High-efficiency TALEN-based gene editing produces disease-resistant rice. Nature Biotechnology 30:390. https://doi.org/10.1038/nbt.2199

Lin Q, Zong Y, Xue C, Wang S, Jin S, Zhu Z, ... Gao C (2020). Prime genome editing in rice and wheat. Nature Biotechnology 38:582-585. https://doi.org/10.1038/s41587-020-0455-x

Liu J, Nannas NJ, Fu F-f, Shi J, Aspinwall B, Parrott WA, Dawe RK (2019). Genome-scale sequence disruption following biolistic transformation in rice and maize. The Plant Cell 31(2):368-383. https://doi.org/10.1105/tpc.18.00613

Lopez-Obando M, Hoffmann B, Gery C, Guyon-Debast A, Teoule E, Rameau C, … Nogue F (2016). Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens. G3: Genes, Genomes, Genetics 6:3647-3653. https://doi.org/10.1534/g3.116.033266

Lu Y, Zhu J-K (2017). Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Molecular Plant 10(3):523-525. https://doi.org/10.1016/j.molp.2016.11.013

Lv C, Huang Y, Sun W, Yu L, Zhu J (2020). Response of rice yield and yield components to elevated [CO2]: a synthesis of updated data from FACE experiments. European Journal of Agronomy 112:125961. https://doi.org/10.1016/j.eja.2019.125961

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

Ma L, Zhu F, Li Z, Zhang J, Li X, Dong J, Wang T (2015). TALENbased mutagenesis of lipoxygenase LOX3 enhances the storagetolerance of rice (Oryza sativa) seeds. PLoS One 10:e0143877. https://doi.org/10.1371/journal.pone.0143877

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, ... Liu YG (2015). A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular Plant 8:1274-1284. https://doi.org/10.1016/j.molp.2015.04.007

Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK (2013). Application of the CRISPR-Cas system for efficient genome engineering in plants. Molecular Plant 6:2008-2011. https://doi.org/10.1093/mp/sst121

Mao T, Zhu M, Sheng Z, Shao G, Jiao G, Mawia AM, ... Hu P (2021). Effects of grain shape genes editing on appearance quality of erect-panicle geng/japonica rice. Rice 14(1):1-7. https://doi.org/10.1186/s12284-021-00517-5

Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, . . . Qu L-J (2013). Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research 23(10):1233-1236. https://doi.org/10.1038/cr.2013.123

Mishra R, Joshi RK, Zhao K (2018). Genome editing in rice: recent advances, challenges, and future implications. Frontiers in Plant Science 9(1361). https://doi.org/10.3389/fpls.2018.01361

Mishra R, Zhao K (2018). Genome editing technologies and their applications in crop improvement. Plant Biotechnology Reports 12:57-68. https://doi.org/10.1007/s11816-018-0472-0

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

Miura K, Ikeda M, Matsubara A, Song X-J, Ito M, Asano K, . . . Ashikari M (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nature Genetics 42(6):545-549. https://doi.org/10.1038/ng.592

Monsur MB, Shao G, Lv Y, Ahmad S, Wei X, Hu P, Tang S (2020). Base editing: the ever expanding clustered regularly interspaced short palindromic repeats (CRISPR) tool kit for precise genome editing in plants. Genes 11(4):466. https://doi.org/10.3390/genes11040466

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

Nishitani C, Hirai N, Komori S, Wada M, Okada K, Osakabe K, ... Osakabe Y (2016). Efficient genome editing in apple using a CRISPR/Cas9 system. Scientific Reports 6(1):1-8. https://doi.org/10.1038/srep31481

Nordin Y (2008). Golden rice and other biofortified food crops for developing countries: challenges and potential. FAO, Rome, Italy.

Osakabe K, Osakabe Y, Toki S (2010). Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proceedings of the National Academy of Sciences 107:12034-12039. https://doi.org/10.1073/pnas.1000234107

Potrykus I (2008, September). Golden Rice—from idea to reality. Bertebos Prize lecture. In: Bertebos Conf., 7–9 September.

Petolino JF, Worden A, Curlee K, Connell J, Moynahan TLS, Larsen C, Russell S (2010). Zinc finger nuclease-mediated transgene deletion. Plant Molecular Biology 73:617-628. https://doi.org/10.1111/pbi.12941

Puchta H (2004). The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. Journal of Experimental Botany 56:1-14. https://doi.org/10.1093/jxb/eri025

Puchta H (2017). Applying CRISPR/Cas for genome engineering in plants: The best is yet to come. Current Opinion in Plant Biology 36:1-8. https://doi.org/10.1016/j.pbi.2016.11.011

Pyott DE, Sheehan E, Molnar A (2016). Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Molecular Plant Pathology 17:1276-1288. https://doi.org.10.1111/mpp.12417

Rai KM, Ghose K, Rai A, Singh H, Srivastava R, Mendu V (2018). Genome engineering tools in plant synthetic biology. In: Current Developments in Biotechnology and Bioengineering. Elsevier, pp 47-73.

Rees HA, Liu DR (2018). Base editing: precision chemistry on the genome and transcriptome of living cells. Nature Reviews Genetics 19(12):770-788. https://doi.org/10.1038/s41576-018-0059-1

Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, … Morell M (2006). High-amylose wheat generated by RNA interference improves indicesof large-bowel health in rats. Proceedings of the National Academy of Sciences 103:3546-3551. https://doi.org/10.1073/pnas.0510737103

Ren C, Liu X, Zhang Z, Wang Y, Duan W, Li S, Liang Z (2016). CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay Vitis vinifera L. Scientific Reports 6:32289. https://doi.org/10.1038/srep32289

Riaz A, Kanwal F, Ahmad I, Ahmad S, Farooq A, Madsen CK, … Alqudah AM (2022). New hope for genome editing in cultivated grasses: CRISPR variants and application. Frontiers in Genetics 13:866121. https://doi.org/10.3389/fgene.2022.866121

Romero FM, Gatica-Arias A (2019). CRISPR/Cas9: development and application in rice breeding. Rice Science 26(5):265-281. https://doi.org/10.1016/j.rsci.2019.08.001

Sauer NJ, Narvaez-Vasquez J, Mozoruk J, Miller RB, Warburg ZJ, Woodward MJ, … Sanders SL (2016). Oligonucleotide mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiology 170:1917-1928. https://doi.org/10.1104/pp.15.01696

Sedeek KEM, Mahas A, Mahfouz M (2019). Plant genomeengineering for targeted improvement of crop traits. Frontiers in Plant Science 10:114. https://doi.org/10.3389/fpls.2019.00114

Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015). Creation of fragrant rice by targeted knockout of the Os BADH 2 gene using TALEN technology. Plant Biotechnology Journal 13:791-800. https://doi.org/10.1111/pbi.12312

Shan Q, Wang Y, Li J, Gao C (2014). Genome editing in rice and wheat using the CRISPR/Cas system. Nature Protocols 9(10):2395-2410. https://doi.org/10.1038/nprot.2014.157

Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, … Qiu JL (2013a). Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology 31:686-688. https://doi.org/10.1038/nbt.2650

Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, . . . Zheng X (2013). Rapid and efficient gene modification in rice and Brachypodium using TALENs. Molecular Plant 6(4):1365-1368. https://doi.org/10.1093/mp/sss162

Shao G, Xie L, Jiao G, Wei X, Sheng Z, Tang S, ... Hu P (2017). CAS9-mediated editing of the fragrant gene Badh2 in rice. Chinese Journal of Rice Science 31:216-222. https://doi.org/10.16819/j.1001-7216.2017.6098

Shen L, Li J, Fu Y, Wang J, Hua Y, Jiao X, Yan C, Wang K (2017). Orientation improvement of grain lengthand grain number in rice by using CRISPR/Cas9 system. Chinese Journal of Rice Science 31:223-231.

Shukla VK, Doyon Y, Miller JC, Dekelver RC, Moehle EA, Worden SE, … Urnov FD (2009). Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437-441. https://doi.org/10.1038/nature07992

Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, ... Kondo A (2017). Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidinedeaminase fusion. Nature Biotechnology 35:441. https://doi.org/10.1038/nbt.3833

Sun Y, Jiao G, Liu Z, Zhang X, Li J, Guo X, ... Xia L (2017). Generation of highamylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Frontiers in Plant Science 8:298. https://doi.org/10.3389/fpls.2017.00298

Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T (2014). CRISPR/ Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant and Cell Physiology 55:475-481. https://doi.org/10.1093/pcp/pcu014

Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015). Targeted mutagenesis, precise gene editing and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiology 169:931-945. https://doi.org.10.1104/pp.15.00793

Stadler LJ (1928). Genetic effects of X-rays in maize. Proceedings of the National Academy of Sciences 14(1):69-75. https://doi.org/10.1073/pnas.14.1.69

Tabassum J, Ahmad S, Hussain B, Mawia AM, Zeb A, Ju L (2021). Applications and potential of genome-editing systems in rice improvement: current and future perspectives. Agronomy 11(7):1359. https://doi.org/10.3390/agronomy11071359

Tang X, Sretenovic S, Ren Q, Jia X, Li M, Fan T, . . . Liu L (2020). Plant prime editors enable precise gene editing in rice cells. Molecular Plant 13(5):667-670. https://doi.org/10.1016/j.molp.2020.03.010

Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, ... Zhao B (2017). Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd accumulating indica rice without compromising yield. Scientific Reports 7:14438. https://doi.org/10.1038/s41598-017-14832-9

Tian S, Jiang L, Gao Q, Zhang J, Zong M, Zhang H, … Liu F (2017). Efficient CRISPR/ Cas9-based gene knockout in watermelon. Plant Cell Reports 36:399-406. https://doi.org.10.1007/s00299-016-2089-5

Townson J (2017). Recent developments in genome editing for potential use in plants. Bioscience Horizons: The International Journal of Student Research 10. https://doi.org/10.1093/biohorizons/hzx016

Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009). High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442-445. https://doi.org/10.1038/nature07845

Urnov FD, Rebar E J, Holmes MC, Zhang HS, Gregory PD (2010). Genome editing with engineered zinc finger nucleases. Nature Reviews Genetics 11(9):636-646. https://doi.org/10.1038/nrg2842

Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, . . . Qian Q (2012). Control of grain size, shape and quality by OsSPL16 in rice. Nature Genetics 44(8):950. https://doi.org/10.1038/ng.2327

Wang C, Liu Q, Shen Y, Hua Y, Wang J, Lin J, ... Wang K (2019). Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nature Biotechnology 37:283-286. https://doi.org/10.1038/s41587-018-0003-0

Wang W, Hu B, Yuan D, Liu Y, Che R, Hu Y, . . . Chu C (2018). Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. The Plant Cell 30(3):638-651. https://doi.org.10.1105/tpc.17.00809

Wang M, Wang S, Liang Z, Shi W, Gao C, Xia G (2017b). From genetic stock to genome editing: gene exploitation in wheat. Trends in Biotechnology 36:160-172. https://doi.org/10.1016/j.tibtech.2017.10.002

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

Waltz E (2016). CRISPR-edited crops free to enter market, skip regulation. Nature Biotechnology 34:582. https://doi.org/10.1038/nbt0616-582

Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, … Kim JS (2015). DNA-free genome editing in plants with preassembled CRISPR Cas9 ribonucleoproteins. Nature Biotechnology 33:1162-1164. https://doi.org/10.1038/nbt.3389

Wang S, Zhang S, Wang W, Xiong X, Meng F, Cui X (2015b). Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Reports 34:1473-1476. https://doi.org/10.1007/s00299-015-1816-7

Wenefrida I, Utomo HS, Blanche SB, Linscombe SD (2009). Enhancing essential amino acids and health benefit components in grain crops for improved nutritional values. Recent Patents on DNA & Gene Sequences 3:219-225. https://doi.org/10.2174/187221509789318405

Xu R, Li J, Liu X, Shan T, Qin R, Wei P (2020). Development of a plant prime editing system for precise editing in the rice genome. Plant Communications 1(3):100043. https://doi.org/10.1016/j.xplc.2020.100043

Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, . . . Yang J (2016). Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. Journal of Genetics and Genomics 43(8):529-532. https://doi.org/10.1016/j.jgg.2016.07.003

Xu R-F, Li H, Qin R-Y, Li J, Qiu C-H, Yang Y-C, ... Yang JB (2015). Generation of inheritable and “transgene clean” targeted genome-modifiedrice in later generations using the CRISPR/Cas9 system. Scientific Reports 5:11491. https://doi.org.10.1038/srep11491

Xu Y, Wang F, Chen Z, Wang J, Li W, Fan F, . . . Yang J (2020). CRISPR/Cas9‐targeted mutagenesis of the OsROS1 gene induces pollen and embryo sac defects in rice. Plant Biotechnology Journal 18(10):1999. https://doi.org/10.1111/pbi.13388

Xu W, Zhang C, Yang Y, Zhao S, Kang G, He X, ... Yang J (2020). Versatile nucleotides substitution in plant using an improved prime editing system. Molecular Plant 13:675-678. https://doi.org/10.1016/j.molp.2020.03.012

Zafra MP, Schatoff EM, Katti A, Foronda M, Breinig M, Schweitzer AY, ... Dow LE (2018). Optimized base editors enable efficient editing in cells, organoids and mice. Nature Biotechnology 36:888-893. https://doi.org/10.1038/nbt.4194

Zaidi SS, Mukhtar MS, Mansoor S (2018). Genome editing: targeting susceptibility genes for plant disease resistance. Trends in Biotechnology 36:898-906. https://doi.org/10.1016/j.tibtech.2018.04.005

Zaidi SS, Mansoor S (2017). Viral vectors for plant genome engineering. Frontiers in Plant Science 8:539. https://doi.org/10.3389/fpls.2017.00539

Zeng Y, Wen J, Zhao W, Wang Q, Huang W (2020). Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR–Cas9 system. Frontiers in Plant Science 10:1663. https://doi.org/10.3389/fpls.2019.01663

Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, ... Gao C (2017). Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nature Biotechnology 35:438-440. https://doi.org/10.1038/nbt.3811

Zhang B, Yang X, Yang C, Li M, Guo Y (2016a). Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in Petunia. Scientific Reports 6:20315. https://doi.org/10.1038/srep20315

Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, ... Gao C (2016). Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nature Communications 7:12617. https://doi.org/10.1038/ncomms12617

Zhang H, Zhang J, Lang Z, Botella JR, Zhu JK (2017). Genome editing—principles and applications for functional genomics research and crop improvement. Critical Review in Plant Science 36:291-309. https://doi.org/10.1080/07352689.2017.1402989

Zhang F, Maeder ML, Unger-Wallaced E, Hoshaw JP, Reyon D, Christian M, ... (2010). High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. roceedings of the National Academy of Sciences 107:12028-12033. https://doi.org/10.1073/pnas.0914991107

Zhou H, He M, Li J, Chen L, Huang Z, Zheng S, . . . Zhao B (2016). Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Scientific Reports 6(1):1-12. https://doi.org/10.1038/srep37395

Zhang Y, Pribil M, Palmgren M, Gao C (2020). A CRISPR way for accelerating improvement of food crops. Nature Food 1:200-205. https://doi.org/10.1038/s43016-020-0051-8



How to Cite

ZEB, A., AHMAD, S., TABBASUM, J., SHENG, Z., & HU, P. (2022). Rice grain yield and quality improvement via CRISPR/Cas9 system: an updated review. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(3), 12388. https://doi.org/10.15835/nbha50312388



Review Articles
DOI: 10.15835/nbha50312388