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GM Crops & Food
Biotechnology in Agriculture and the Food Chain
Volume 14, 2023 - Issue 1
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Review

Putting CRISPR-Cas system in action: a golden window for efficient and precise genome editing for crop improvement

Arooj Tariqa Department of Biotechnology, School of Biosciences and Biotechnology, BGSB University, Rajouri, J&K, IndiaView further author information
,
Muntazir Mushtaqb MS Swaminathan School of Agriculture, Shoolini University of Biotechnology and Management Sciences, Bajhol, Solan, Himachal Pradesh, IndiaView further author information
,
Huwaida Yaqooba Department of Biotechnology, School of Biosciences and Biotechnology, BGSB University, Rajouri, J&K, IndiaView further author information
,
Basharat Ahmad Bhatc Department of Bioresources, Amar Singh College Campus, Cluster University, Srinagar, IndiaView further author information
,
Sajad Majeed Zargard Proteomics Laboratory, Division of Plant Biotechnology, (SKUAST-K), Shalimar, Kashmir, IndiaCorrespondence[email protected]
View further author information
,
Ali Razae College of Agriculture, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-5120-2791View further author information
ORCID Icon,
Sajad Alif Department of Biotechnology, Yeungnam University, Gyeongsan, South KoreaView further author information
,
Sidra Charaghg State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences (CAAS), Hangzhou, Zhejiang, ChinaORCID Iconhttps://orcid.org/0000-0002-8077-7324View further author information
ORCID Icon,
Muhammad Salman Mubarikh Department of Biotechnology, University of Narowal, Narowal, PakistanORCID Iconhttps://orcid.org/0000-0001-6522-4660View further author information
ORCID Icon,
Qamar U Zamani Yazhou Bay Seed Laboratory, Sanya Nanfan Research Institute of Hainan University, Sanya, China;j College of Tropical Crops, Hainan University, Haikou, ChinaORCID Iconhttps://orcid.org/0000-0002-2665-7436View further author information
ORCID Icon,
PV Vara Prasadk Department of Agronomy, Kansas State University, Manhattan, KS, USAORCID Iconhttps://orcid.org/0000-0001-6632-3361View further author information
ORCID Icon &
Rakeeb Ahmad Mirl Department of Biotechnology, School of Life Sciences, Central University of Kashmir, Ganderbal, J&K, IndiaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-7254-2349View further author information
ORCID Icon show all
Pages 1-27 | Received 11 Jan 2023, Accepted 24 May 2023, Published online: 08 Jun 2023

References

  • Farooq MS, Uzair M, Raza A, Habib M, Xu Y, Yousuf M, Yang SH, Ramzan Khan M. Uncovering the Research Gaps to Alleviate the Negative Impacts of Climate Change on Food Security: a Review. Front Plant Sci. 2022;13:927535. doi:10.3389/fpls.2022.927535.
  • Scheben A, Yuan Y, Edwards D. Advances in genomics for adapting crops to climate change. Current Plant Biology. 2016;6:2–10. doi:10.1016/j.cpb.2016.09.001.
  • Kang Y, Khan S, Ma X. Climate change impacts on crop yield, crop water productivity and food security–A review. Progress In Natural Science. 2009;19(12):1665–74. doi:10.1016/j.pnsc.2009.08.001.
  • Rivero RM, Mittler R, Blumwald E, Zandalinas SI. Developing climate‐resilient crops: improving plant tolerance to stress combination. The Plant Journal. 2022;109(2):373–89. doi:10.1111/tpj.15483.
  • Zandalinas SI, Fritschi FB, Mittler R. Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci. 2021;26(6):588–99. doi:10.1016/j.tplants.2021.02.011.
  • Raza A, Charagh S, Najafi-Kakavand S, Abbas S, Shoaib Y, Anwar S, Sharifi S, Lu G, Siddique KHM. Role of phytohormones in regulating cold stress tolerance: physiological and molecular approaches for developing cold-smart crop plants. Plant Stress. 2023;8:100152. doi:10.1016/j.stress.2023.100152.
  • Oladosu Y, Rafii MY, Abdullah N, Hussin G, Ramli A, Rahim HA, Miah G, Usman M. Principle and application of plant mutagenesis in crop improvement: a review. Biotechnol Biotechnol Equip. 2016;30(1):1–16. doi:10.1080/13102818.2015.1087333.
  • Nasti RA, Voytas DF. Attaining the promise of plant gene editing at scale. Proc Natl Acad Sci. 2021;118(22). doi:10.1073/pnas.2004846117.
  • Yu HQ, Sun FA, Feng WQ, Lu FZ, Li WC, Fu FL. The BES1/BZR1 transcription factors regulate growth, development and stress resistance in plants. Hereditas. 2019;41(3):206–14. doi:10.16288/j.yczz.18-253.
  • Yu H, Feng W, Sun F, Zhang Y, Qu J, Liu B, Lu F, Yang L, Fu F, Li W. Cloning and characterization of BES1/BZR1 transcription factor genes in maize. Plant Growth Regul. 2018;86(2):235–49. doi:10.1007/s10725-018-0424-2.
  • Yu H, Khalid MHB, Lu F, Sun F, Qu J, Liu B, Li W, Fu F. Isolation and identification of a vegetative organ-specific promoter from maize. Physiol Mol Biol Plants. 2019;25(1):277–87. doi:10.1007/s12298-018-0546-z.
  • Sun F, Ding L, Feng W, Cao Y, Lu F, Yang Q, Li W, Lu Y, Shabek N, Fu F, et al. Maize transcription factor ZmBES1/BZR1-5 positively regulates kernel size. J Exp Bot. 2021;72(5):1714–26. doi:10.1093/jxb/eraa544.
  • Sun F, Yu H, Qu J, Cao Y, Ding L, Feng W, Khalid MHB, Li W, Fu F. Maize ZmBES1/BZR1-5 decreases ABA sensitivity and confers tolerance to osmotic stress in transgenic Arabidopsis. Int J Mol Sci. 2020;21(3):996. doi:10.3390/ijms21030996.
  • Lu F, Li W, Peng Y, Cao Y, Qu J, Sun F, Yang Q, Lu Y, Zhang X, Zheng L, et al. ZmPP2C26 alternative splicing variants negatively regulate drought tolerance in maize. Front Plant Sci. 2022;13:871. doi:10.3389/fpls.2022.851531.
  • Yaqoob H, Tariq A, Bhat BA, Bhat KA, Nehvi IB, Raza A, Djalovic I, Prasad PV, Mir RA. Integrating genomics and genome editing for orphan crop improvement: a bridge between orphan crops and modern agriculture system. GM Crops & Food. 2023;14(1):1–20. doi:10.1080/21645698.2022.2146952.
  • Li M, Liu J-X, Deng Y-J, Xu Z-S, Xiong A-S. Heterologous expression of Arabidopsis thaliana rty gene in strawberry (Fragaria× ananassa Duch.) improves drought tolerance. BMC Plant Biol. 2021;21(1):1–20. doi:10.1186/s12870-021-03236-7.
  • Chen K, Gao C. Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep. 2014;33(4):575–83. doi:10.1007/s00299-013-1539-6.
  • Xia L, Wang K, Zhu JK. The power and versatility of genome editing tools in crop improvement. J Integr Plant Biol. 2021;63(9):1591. doi:10.1111/jipb.13160.
  • Lowder L, Malzahn A, Qi Y. Rapid evolution of manifold CRISPR systems for plant genome editing. Front Plant Sci. 2016;7:1683. doi:10.3389/fpls.2016.01683.
  • Zhu C, Bortesi L, Baysal C, Twyman RM, Fischer R, Capell T, Schillberg S, Christou P. Characteristics of genome editing mutations in cereal crops. Trends Plant Sci. 2017;22(1):38–52. doi:10.1016/j.tplants.2016.08.009.
  • Rischer H, Oksman-Caldentey K-M. Unintended effects in genetically modified crops: revealed by metabolomics? Trends Biotechnol. 2006;24(3):102–04. doi:10.1016/j.tibtech.2006.01.009.
  • Mubarik MS, MAJEED S, KHAN SH, DU X, FRELICHOWSKI JE, HINZE L, AZHAR MT. Reforming cotton genes: from elucidation of DNA structure to genome editing. Turk J Agric For. 2021;45(6):691–703. doi:10.3906/tar-2012-64.
  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–23. doi:10.1126/science.1231143.
  • Zhang H, Zhang J, Lang Z, Botella JR, Zhu J-K. Genome editing—principles and applications for functional genomics research and crop improvement. CRC Crit Rev Plant Sci. 2017;36(4):291–309. doi:10.1080/07352689.2017.1402989.
  • Toda E, Koiso N, Takebayashi A, Ichikawa M, Kiba T, Osakabe K, Osakabe Y, Sakakibara H, Kato N, Okamoto T. An efficient DNA-and selectable-marker-free genome-editing system using zygotes in rice. Nature Plants. 2019;5(4):363–68. doi:10.1038/s41477-019-0386-z.
  • Wurtzel ET, Vickers CE, Hanson AD, Millar AH, Cooper M, Voss-Fels KP, Nikel PI, Erb TJ. Revolutionizing agriculture with synthetic biology. Nat Plants. 2019;5(12):1207–10. doi:10.1038/s41477-019-0539-0.
  • Zaman QU, Li C, Cheng H, Hu Q. Genome editing opens a new era of genetic improvement in polyploid crops. null. 2019;7(2):141–50. doi:10.1016/j.cj.2018.07.004.
  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186(2):757–61. doi:10.1534/genetics.110.120717.
  • Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, Anders C, Hauer M, Zhou K, Lin S, et al. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science. 2014;343(6176). doi:10.1126/science.1247997.
  • Nidhi S, Anand U, Oleksak P, Tripathi P, Lal JA, Thomas G, Kuca K, Tripathi V. Novel CRISPR–Cas Systems: an Updated Review of the Current Achievements, Applications, and Future Research Perspectives. Int J Mol Sci. 2021;22(7):3327. doi:10.3390/ijms22073327.
  • Zhang K, Raboanatahiry N, Zhu B, Li M. Progress in genome editing technology and its application in plants. Front Plant Sci. 2017;8:177. doi:10.3389/fpls.2017.00177.
  • Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu J-K. Application of the CRISPR–Cas system for efficient genome engineering in plants. Mol Plant. 2013;6(6):2008. doi:10.1093/mp/sst121.
  • Schornack S, Moscou MJ, Ward ER, Horvath DM. Engineering plant disease resistance based on TAL effectors. Annu Rev Phytopathol. 2013;51:383–406.
  • Lakota J. Synthetic Biology-Friend or Foe? What Kind of Threats Should We Expect? Вестник войск РХБ защиты. 2021;5:103–22.
  • Liang Z, Zhang K, Chen K, Gao C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. Journal Of Genetics And Genomics. 2014;41(2):63–68. doi:10.1016/j.jgg.2013.12.001.
  • Mahfouz MM, Piatek A, Stewart CN Jr. Genome engineering via TALENs and CRISPR/Cas9 systems: challenges and perspectives. Plant Biotechnol J. 2014;12(8):1006–14. doi:10.1111/pbi.12256.
  • Li C, Brant E, Budak H, Zhang B. CRISPR/Cas: a Nobel Prize award-winning precise genome editing technology for gene therapy and crop improvement. J Zhejiang Univ-Sc B. 2021;22(4):253–84.
  • Zhu H, Li C, Gao C. Applications of CRISPR–Cas in agriculture and plant biotechnology. Nat Rev Mol Cell Biol. 2020;21(11):661–77. doi:10.1038/s41580-020-00288-9.
  • Walawage SL, Zaini PA, Mubarik MS, Martinelli F, Balan B, Caruso T, Leslie CA, Dandekar AM. Deploying genome editing tools for dissecting the biology of nut trees. Front Sustain Food Syst. 2019;3:100. doi:10.3389/fsufs.2019.00100.
  • Hassan MM, Zhang Y, Yuan G, De K, Chen J-G, Muchero W, Tuskan GA, Qi Y, Yang X. Construct design for CRISPR/Cas-based genome editing in plants. Trends Plant Sci. 2021;26(11):1133–52. doi:10.1016/j.tplants.2021.06.015.
  • Ding Y, Li H, Chen L-L, Xie K. Recent advances in genome editing using CRISPR/Cas9. Front Plant Sci. 2016;7:703. doi:10.3389/fpls.2016.00703.
  • Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu J-L, Gao C. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun. 2016;7(1):1–8. doi:10.1038/ncomms12617.
  • Xing H-L, Dong L, Wang Z-P, Zhang H-Y, Han C-Y, Liu B, Wang X-C, Chen Q-J. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14(1):1–12. doi:10.1186/s12870-014-0327-y.
  • Wang S, Zhang S, Wang W, Xiong X, Meng F, Cui X. Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep. 2015;34(9):1473–76. doi:10.1007/s00299-015-1816-7.
  • Andersson M, Turesson H, Nicolia A, Fält A-S, Samuelsson M, Hofvander P. Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep. 2017;36(1):117–28. doi:10.1007/s00299-016-2062-3.
  • Gao W, Long L, Tian X, Xu F, Liu J, Singh PK, Botella JR, Song C. Genome editing in cotton with the CRISPR/Cas9 system. Front Plant Sci. 2017;8:1364. doi:10.3389/fpls.2017.01364.
  • Braatz J, Harloff H-J, Mascher M, Stein N, Himmelbach A, Jung C. CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploid oilseed rape (Brassica napus). Plant Physiol. 2017;174(2):935–42. doi:10.1104/pp.17.00426.
  • Yang H, Wu J-J, Tang T, Liu K-D, Dai C. Crispr/cas9-mediated genome editing efficiently creates specific mutations at multiple loci using one sgRNA in Brassica napus. null. 2017;7(1):1–13. doi:10.1038/s41598-017-07871-9.
  • Zaman QU, Wen C, Yuqin S, Mengyu H, Desheng M, Jacqueline B, Baohong Z, Chao L, Qiong H. Characterization of SHATTERPROOF homoeologs and CRISPR-Cas9-mediated genome editing enhances pod-shattering resistance in Brassica napus L. The CRISPR Journal. 2021;4(3):360–70. doi:10.1089/crispr.2020.0129.
  • Zaman QU, Chu W, Hao M, Shi Y, Sun M, Sang S-F, Mei D, Cheng H, Liu J, Li C, et al. Crispr/cas9-mediated multiplex genome editing of JAGGED gene in Brassica napus L. Biomolecules. 2019;9(11):725. doi:10.3390/biom9110725.
  • Rasheed A, Gill RA, Hassan MU, Mahmood A, Qari S, Zaman QU, Ilyas M, Aamer M, Batool M, Li H, et al. A critical review: recent advancements in the use of CRISPR/Cas9 technology to enhance crops and alleviate global food crises. Curr Issues Mol Biol. 2021;43(3):1950–76. doi:10.3390/cimb43030135.
  • Jang G, Joung YH. Crispr/cas-mediated genome editing for crop improvement: current applications and future prospects. Plant Biotechnol Rep. 2019;13(1):1–10. doi:10.1007/s11816-018-0509-4.
  • Hille F, Richter H, Wong SP, Bratovič M, Ressel S, Charpentier E. The biology of CRISPR-Cas: backward and forward. Cell. 2018;172(6):1239–59. doi:10.1016/j.cell.2017.11.032.
  • Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA. 2012;109(39):E2579–E86. doi:10.1073/pnas.1208507109.
  • Nierzwicki L, Arantes PR, Saha A, Palermo G. Establishing the allosteric mecanism in CRISPR-Cas9. Wiley Interdiscip Rev Comput Mol Sci. 2020;e1503.
  • Koonin EV, Makarova KS, Zhang F. Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol. 2017;37:67–78.
  • Carabias A, Fuglsang A, Temperini P, Pape T, Sofos N, Stella S, Erlendsson S, Montoya G. Structure of the mini-RNA-guided endonuclease CRISPR-Cas12j3. Nat Commun. 2021;12(1):1–12. doi:10.1038/s41467-021-24707-3.
  • Jiang F, Doudna JA. CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys. 2017;46(1):505–29. doi:10.1146/annurev-biophys-062215-010822.
  • Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature. 2011;471(7340):602–07. doi:10.1038/nature09886.
  • Garneau JE, Dupuis M-È, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature. 2010;468(7320):67–71. doi:10.1038/nature09523.
  • Chen F, Ding X, Feng Y, Seebeck T, Jiang Y, Davis GD. Targeted activation of diverse CRISPR-Cas systems for mammalian genome editing via proximal CRISPR targeting. Nat Commun. 2017;8(1):1–12.
  • Schmid-Burgk JL, Gao L, Li D, Gardner Z, Strecker J, Lash B, Zhang F. Highly parallel profiling of Cas9 variant specificity. Mol Cell. 2020;78(4):794–800.e8. doi:10.1016/j.molcel.2020.02.023.
  • Anzalone AV, Koblan LW, Liu DR. Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors. Nat Biotechnol. 2020;38:824–44.
  • Jiang F, Taylor DW, Chen JS, Kornfeld JE, Zhou K, Thompson AJ, Nogales E, Doudna JA. Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science. 2016;351(6275):867–71. doi:10.1126/science.aad8282.
  • Szczelkun MD, Tikhomirova MS, Sinkunas T, Gasiunas G, Karvelis T, Pschera P, Siksnys V, Seidel R. Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. Proc Natl Acad Sci USA. 2014;111(27):9798–803. doi:10.1073/pnas.1402597111.
  • Pacesa M, Lin CH, et al. Structural basis for Cas9 off-target activity. Cell. 2022; 185(22): 4067–4081.
  • Jiang F, Zhou K, Ma L, Gressel S, Doudna JA. A Cas9–guide RNA complex preorganized for target DNA recognition. Science. 2015;348(6242):1477–81. doi:10.1126/science.aab1452.
  • Sternberg SH, LaFrance B, Kaplan M, Doudna JA. Conformational control of DNA target cleavage by CRISPR–Cas9. Nature. 2015;527(7576):110–13. doi:10.1038/nature15544.
  • Swartjes T, Staals RHJ, van der Oost J. Editor’s cut: dNA cleavage by CRISPR RNA-guided nucleases Cas9 and Cas12a. Biochem Soc Trans. 2020;48(1):207–19. doi:10.1042/BST20190563.
  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. science. Science. 2012;337(6096):816–21. doi:10.1126/science.1225829.
  • Babu K, Kathiresan V, Kumari P, Newsom S, Parameshwaran HP, Chen X, Liu J, Qin PZ, Rajan R. Coordinated Actions of Cas9 HNH and RuvC Nuclease Domains are Regulated by the Bridge Helix and the Target DNA Sequence. Biochemistry. 2021;60(49):3783–800. doi:10.1021/acs.biochem.1c00354.
  • Nishimasu H, Ran F, Hsu P, Konermann S, Shehata S, Dohmae N, Ishitani R, Zhang F, Nureki O. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell. 2014;156(5):935–49. doi:10.1016/j.cell.2014.02.001.
  • Molla KA, Sretenovic S, Bansal KC, Qi Y. Precise plant genome editing using base editors and prime editors. Nat Plants. 2021;7(9):1166–87. doi:10.1038/s41477-021-00991-1.
  • Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823–26. doi:10.1126/science.1232033.
  • Cho SW, Kim S, Kim JM, Kim JS. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol. 2013;31(3):230–32.
  • Wang G, Li J. Review, analysis, and optimization of the CRISPR Streptococcus pyogenes Cas9 system. Medicine In Drug Discovery. 2021;9:100080.
  • Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, Zetsche B, Shalem O, Wu X, Makarova KS. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520(7546):186–91.
  • Esvelt KM, Mali P, Braff JL, Moosburner M, Yaung SJ, Church GM. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods. 2013;10(11):1116–21. doi:10.1038/nmeth.2681.
  • Hou Z, Zhang Y, Propson NE, Howden SE, Chu L-F, Sontheimer EJ, Thomson JA. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci USA. 2013;110(39):15644–49. doi:10.1073/pnas.1313587110.
  • Edraki A, Mir A, Ibraheim R, Gainetdinov I, Yoon Y, Song C-Q, Cao Y, Gallant J, Xue W, Rivera-Pérez JA, et al. A compact, high-accuracy Cas9 with a dinucleotide PAM for in vivo genome editing. Mol Cell. 2019;73(4):714–26.e4. doi:10.1016/j.molcel.2018.12.003.
  • Kim E, Koo T, Park SW, Kim K, Cho HY, Song DW, Lee KJ, Jung, MH, Kim S. In vivo genome editing with a small Cas9 orthologue derived from Campylobacter jejuni. Nat Commun. 2017;8(1):1–12.
  • Harrington LB, Paez-Espino D, Staahl BT, Chen JS, Doudna JA. A thermostable Cas9 with increased lifetime in human plasma. Nat Commun. 2017;8(1):1–8.
  • Makarova KS, Wolf YI, Iranzo J, Shmakov SA, Alkhnbashi OS, Brouns SJJ, Charpentier E, Cheng D, Haft DH, Horvath P, et al. Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol. 2020;18(2):67–83. doi:10.1038/s41579-019-0299-x.
  • Zetsche B, Gootenberg J, Abudayyeh O, Slaymaker I, Makarova K, Essletzbichler P, Volz S, Joung J, van der Oost J, Regev A, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163(3):759–71. doi:10.1016/j.cell.2015.09.038.
  • Zetsche B, Heidenreich M, Mohanraju P, Fedorova I, Kneppers J, DeGennaro EM, Winblad N, Choudhury SR, Abudayyeh OO, Gootenberg JS, et al. Multiplex gene editing by CRISPR–Cpf1 using a single crRNA array. Nat Biotechnol. 2017;35(1):31–34. doi:10.1038/nbt.3737.
  • Yan WX, Hunnewell P, Alfonse LE, Carte JM, Keston-Smith E, Sothiselvam S, Garrity AJ, Chong S, Makarova KS, Koonin EV, et al. Functionally diverse type V CRISPR-Cas systems. Science. 2019;363(6422):88–91. doi:10.1126/science.aav7271.
  • Chen JS, Ma E, Harrington LB, Da Costa M, Tian X, Palefsky JM, Doudna JA. CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity. Science. 2018;360(6387):436–39. doi:10.1126/science.aar6245.
  • Wang Q, Alariqi M, Wang F, Li B, Ding X, Rui H, Li Y, Xu Z, Qin L, Sun L, et al. The application of a heat-inducible CRISPR/Cas12b (C2c1) genome editing system in tetraploid cotton (G. hirsutum) plants. Plant Biotechnol J. 2020;18(12):2436–43. doi:10.1111/pbi.13417.
  • Li S, Li J, Du W, Fu J, Sutar S, Zhao Y, Xia, L. Synthesis-dependent repair of Cpf1-induced double strand DNA breaks enables targeted gene replacement in rice. J Exp Bot. 2018;69(20):4715–21.
  • Yu K, Liu Z, Gui H, Geng L, Wei J, Liang D, Lv J, Xu J, Chen X. Highly efficient generation of bacterial leaf blight-resistant and transgene-free rice using a genome editing and multiplexed selection system. BMC Plant Biol. 2021;21(1):1–10. doi:10.1186/s12870-021-02979-7.
  • Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K, et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol. 2017;35(5):441–43. doi:10.1038/nbt.3833.
  • Li C, Zhang R, Meng X, Chen S, Zong Y, Lu C, Qiu J-L, Chen Y-H, Li J, Gao C. Targeted, random mutagenesis of plant genes with dual cytosine and adenine base editors. Nat Biotechnol. 2020;38(7):875–82. doi:10.1038/s41587-019-0393-7.
  • Jin S, Fei H, Zhu Z, Luo Y, Liu J, Gao S, Zhang F, Chen Y-H, Wang Y, Gao C. Rationally designed APOBEC3B cytosine base editors with improved specificity. Mol Cell. 2020;79(5):728–40.e6. doi:10.1016/j.molcel.2020.07.005.
  • Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR. Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature. 2017;551(7681):464–71. doi:10.1038/nature24644.
  • Kang B-C, Yun J-Y, Kim S-T, Shin Y, Ryu J, Choi M, Woo JW, Kim J-S. Precision genome engineering through adenine base editing in plants. Nature Plants. 2018;4(7):427–31. doi:10.1038/s41477-018-0178-x.
  • Li C, Zong Y, Wang Y, Jin S, Zhang D, Song Q, Zhang R, Gao C. Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol. 2018;19(1):1–9. doi:10.1186/s13059-018-1443-z.
  • Hua K, Tao X, Zhu JK. Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J. 2019;17(2):499–504. doi:10.1111/pbi.12993.
  • Gaudelli NM, Lam DK, Rees HA, Solá-Esteves NM, Barrera LA, Born DA, Edwards A, Gehrke JM, Lee S-J, Liquori AJ, et al. Directed evolution of adenine base editors with increased activity and therapeutic application. Nat Biotechnol. 2020;38(7):892–900. doi:10.1038/s41587-020-0491-6.
  • Richter MF, Zhao KT, Eton E, Lapinaite A, Newby GA, Thuronyi BW, Wilson C, Koblan LW, Zeng J, Bauer DE, et al. Phage-assisted evolution of an adenine base editor with improved Cas domain compatibility and activity. Nat Biotechnol. 2020;38(7):883–91. doi:10.1038/s41587-020-0453-z.
  • Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, et al. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature. 2019;576(7785):149–57. doi:10.1038/s41586-019-1711-4.
  • Jiang Y-Y, Chai Y-P, Lu M-H, Han X-L, Lin Q, Zhang Y, Zhang Q, Zhou Y, Wang X-C, Gao C, et al. Prime editing efficiently generates W542L and S621I double mutations in two ALS genes in maize. Genome Biol. 2020;21(1):1–10. doi:10.1186/s13059-020-02170-5.
  • Liu H, Ding Y, Zhou Y, Jin W, Xie K, Chen L-L. CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant. 2017;10(3):530–32. doi:10.1016/j.molp.2017.01.003.
  • Li J, Zhang S, Zhang R, Gao J, Qi Y, Song G, Li W, Li Y, Li G. Efficient multiplex genome editing by CRISPR/Cas9 in common wheat. Plant Biotechnol J. 2021;19(3):427. doi:10.1111/pbi.13508.
  • Wang C, Liu W, Wang G, Li J, Dong L, Han L, Wang Q, Tian J, Yu Y, Gao C, et al. KTN80 confers precision to microtubule severing by specific targeting of katanin complexes in plant cells. Embo J. 2017;36(23):3435–47. doi:10.15252/embj.201796823.
  • Tang X, Zheng X, Qi Y, Zhang D, Cheng Y, Tang A, Voytas D, Zhang Y. A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Mol. Mol Plant. 2016;9(7):1088–91. doi:10.1016/j.molp.2016.05.001.
  • Wang M, Mao Y, Lu Y, Tao X, Zhu J-K. Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol Plant. 2017;10(7):1011–13. doi:10.1016/j.molp.2017.03.001.
  • Doench JG. Am I ready for CRISPR? A user’s guide to genetic screens. Nat Rev Genet. 2018;19(2):67–80. doi:10.1038/nrg.2017.97.
  • Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 2014;343(6166):84–87. doi:10.1126/science.1247005.
  • Lu Y, Ye X, Guo R, Huang J, Wang W, Tang J, Tan L, Zhu J-K, Chu C, Qian Y. Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol Plant. 2017;10(9):1242–45. doi:10.1016/j.molp.2017.06.007.
  • Meng X, Yu H, Zhang Y, Zhuang F, Song X, Gao S, Gao C, Li J. Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Mol. Mol Plant. 2017;10(9):1238–41. doi:10.1016/j.molp.2017.06.006.
  • Jacobs TB, Zhang N, Patel D, Martin GB. Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiol. 2017;174(4):2023–37. doi:10.1104/pp.17.00489.
  • Liu H-J, Jian L, Xu J, Zhang Q, Zhang M, Jin M, Peng Y, Yan J, Han B, Liu J, et al. High-throughput CRISPR/Cas9 mutagenesis streamlines trait gene identification in maize. Plant Cell. 2020;32(5):1397–413. doi:10.1105/tpc.19.00934.
  • Nadakuduti SS, Enciso-Rodríguez F. Advances in genome editing with CRISPR systems and transformation technologies for plant DNA manipulation. Front Plant Sci. 2021;11:2267. doi:10.3389/fpls.2020.637159.
  • Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, Smith I, Sullender M, Ebert BL, Xavier RJ, Root DE. Rational design of highly active sgRnas for CRISPR-Cas9–mediated gene inactivation. Nat Biotechnol. 2014;32(12):1262–67. doi:10.1038/nbt.3026.
  • Sanson KR, Hanna RE, Hegde M, Donovan KF, Strand C, Sullender ME, Vaimberg EW, Goodale A, Root DE, Piccioni F, et al. Optimized libraries for CRISPR-Cas9 genetic screens with multiple modalities. Nat Commun. 2018;9(1):1–15. doi:10.1038/s41467-018-07901-8.
  • Gaillochet C, Develtere W, Jacobs TB. CRISPR screens in plants: approaches, guidelines, and future prospects. Plant Cell. 2021;33(4):794–813. doi:10.1093/plcell/koab099.
  • Chen K, Wang Y, Zhang R, Zhang H, Gao C. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol. 2019;70(1):667–97. doi:10.1146/annurev-arplant-050718-100049.
  • Korotkova AM, Gerasimova SV, Khlestkina EK. Current achievements in modifying crop genes using CRISPR/Cas system. Vavilov J Genet Breed. 2019;23(1):29–37. doi:10.18699/VJ19.458.
  • Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB. Engineering quantitative trait variation for crop improvement by genome editing. Cell. 2017;171(2):470–80.e8. doi:10.1016/j.cell.2017.08.030.
  • Liu Q, Yang F, Zhang J, Liu H, Rahman S, Islam S, Ma W, She M. Application of CRISPR/Cas9 in Crop Quality Improvement. Int J Mol Sci. 2021;22(8):4206. doi:10.3390/ijms22084206.
  • Sarmah BK, Gohain M, Borah BK, Acharjee S. Cisgenesis: engineering Plant Genome by Harnessing Compatible Gene Pools. Genome Engineering For Crop Improvement. 2021. p 193–216.
  • Giudice G, Moffa L, Varotto S, Cardone MF, Bergamini C, De Lorenzis G, Velasco R, Nerva L, Chitarra W. Novel and emerging biotechnological crop protection approaches. Plant Biotechnol J. 2021;19(8):1495–510. doi:10.1111/pbi.13605.
  • Holme IB, Wendt T, Holm PB. Intragenesis and cisgenesis as alternatives to transgenic crop development. Plant Biotechnol J. 2013;11(4):395–407. doi:10.1111/pbi.12055.
  • Cardi T, Varshney R. Cisgenesis and genome editing: combining concepts and efforts for a smarter use of genetic resources in crop breeding. Plant Breeding. 2016;135(2):139–47. doi:10.1111/pbr.12345.
  • Brocken DJ, Tark-Dame M, Dame RT. dCas9: a versatile tool for epigenome editing. Curr Issues Mol Biol. 2018;26(1):15–32. doi:10.21775/cimb.026.015.
  • Hilton IB, D'ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol. 2015;33(5):510–17.
  • Papikian A, Liu W, Gallego-Bartolomé J, Jacobsen SE. Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat Commun. 2019;10(1):1–11. doi:10.1038/s41467-019-08736-7.
  • Paixão JFR, Gillet F-X, Ribeiro TP, Bournaud C, Lourenço-Tessutti IT, Noriega DD, Melo BPD, de Almeida-Engler J, Grossi-de-Sa MF. Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a Histone AcetylTransferase. 2019;9(1):1–9. doi:10.1038/s41598-019-44571-y.
  • Vanblaere T, Flachowsky H, Gessler C, Broggini GAL. Molecular characterization of cisgenic lines of apple ‘Gala’carrying the Rvi6 scab resistance gene. Plant Biotechnol J. 2014;12(1):2–9. doi:10.1111/pbi.12110.
  • Würdig J, Flachowsky H, Saß A, Peil A, Hanke M-V. Improving resistance of different apple cultivars using the Rvi6 scab resistance gene in a cisgenic approach based on the Flp/FRT recombinase system. Mol Breeding. 2015;35(3):1–18. doi:10.1007/s11032-015-0291-8.
  • Jo K-R, Kim C-J, Kim S-J, Kim T-Y, Bergervoet M, Jongsma MA, Visser RG, Jacobsen E, Vossen JH. Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnol. 2014;14(1):1–10. doi:10.1186/1472-6750-14-50.
  • Crisp PA, Bhatnagar-Mathur P, Hundleby P, Godwin ID, Waterhouse PM, Hickey LT. Beyond the gene: epigenetic and cis-regulatory targets offer new breeding potential for the future. Curr Opin Biotechnol. 2022;73:88–94. doi:10.1016/j.copbio.2021.07.008.
  • Duan Y-B, Li J, Qin R-Y, Xu R-F, Li H, Yang Y-C, Ma H, Li L, Wei P-C, Yang J-B. Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol Biol. 2016;90(1–2):49–62. doi:10.1007/s11103-015-0393-z.
  • Li C, Li W, Zhou Z, Chen H, Xie C, Lin Y. A new rice breeding method: cRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene‐free bacterial blight‐resistant rice. Plant Biotechnol J. 2020;18(2):313.
  • Schiml S, Puchta H. Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas. Plant Methods. 2016;12(1):1–9. doi:10.1186/s13007-016-0103-0.
  • Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J. 2017;15(12):1509–19. doi:10.1111/pbi.12733.
  • Oliva R, Ji C, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A, Li T, Eom J-S, Li C, Nguyen H, Liu B, et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol. 2019;37(11):1344–50. doi:10.1038/s41587-019-0267-z.
  • Xu Z, Xu X, Gong Q, Li Z, Li Y, Wang S, Yang Y, Ma W, Liu L, Zhu B, et al. Engineering broad-spectrum bacterial blight resistance by simultaneously disrupting variable TALE-binding elements of multiple susceptibility genes in rice. Mol Plant. 2019;12(11):1434–46. doi:10.1016/j.molp.2019.08.006.
  • Jia H, Orbovic V, Jones JB, Wang N. Modification of the PthA4 effector binding elements in Type I Cs LOB 1 promoter using Cas9/sg RNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4: dCs LOB 1.3 infection. Plant Biotechnol J. 2016;14(5):1291–301. doi:10.1111/pbi.12495.
  • Jia H, Wang N. Generation of homozygous canker‐resistant citrus in the T0 generation using CRISPR‐SpCas9p. Plant Biotechnol J. 2020;18(10):1990. doi:10.1111/pbi.13375.
  • Jia H, Omar AA, Orbović V, Wang N. Biallelic editing of the LOB1 promoter via CRISPR/Cas9 creates canker-resistant ‘Duncan’grapefruit. Phytopathology. 2022;112(2):308–314.
  • Li Q, Sapkota M, van der Knaap E. Perspectives of CRISPR/Cas-mediated cis-engineering in horticulture: unlocking the neglected potential for crop improvement. Horticul Res. 2020;7(1):1–11. doi:10.1038/s41438-020-0258-8.
  • Yan W, Chen D, Kaufmann K. Efficient multiplex mutagenesis by RNA-guided Cas9 and its use in the characterization of regulatory elements in the AGAMOUS gene. Plant Methods. 2016;12(1):1–9. doi:10.1186/s13007-016-0125-7.
  • Liu M, Rehman S, Tang X, Gu K, Fan Q, Chen D, Ma W. Methodologies for improving HDR efficiency. Front Genet. 2019;9:691. doi:10.3389/fgene.2018.00691.
  • Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF. High-frequency, precise modification of the tomato genome. Genome Biol. 2015;16(1):1–15. doi:10.1186/s13059-015-0796-9.
  • Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE. ARGOS 8 variants generated by CRISPR‐Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J. 2017;15(2):207–16. doi:10.1111/pbi.12603.
  • Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A, Boyher A, Starker CG, Bart R, Voytas DF, Taylor NJ. Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol J. 2018;16(7):1275–82. doi:10.1111/pbi.12868.
  • Mohanta TK, Bashir T, Hashem A, Abd_allah E, Bae H. Genome editing tools in plants. Genes. 2017;8(12):399. doi:10.3390/genes8120399.
  • Ahmad S, Tang L, Shahzad R, Mawia AM, Rao GS, Jamil S, Wei C, Sheng Z, Shao G, Wei X, et al. CRISPR-based crop improvements: a way forward to achieve zero hunger. J Agric Food Chem. 2021;69(30):8307–23. doi:10.1021/acs.jafc.1c02653.
  • Zhou H, He M, Li J, Chen L, Huang Z, Zheng S, Zhu L, Ni E, Jiang D, Zhao B, et al. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. . 2016;6(1):1–12. doi:10.1038/srep37395.
  • Rao MJ, Wang L. CRISPR/Cas9 technology for improving agronomic traits and future prospective in agriculture. Planta. 2021;254(4):1–16. doi:10.1007/s00425-021-03716-y.
  • Singh M, Kumar M, Albertsen MC, Young JK, Cigan AM. Concurrent modifications in the three homeologs of Ms45 gene with CRISPR-Cas9 lead to rapid generation of male sterile bread wheat (Triticum aestivum L.). Plant Mol Biol. 2018;97(4–5):371–83. doi:10.1007/s11103-018-0749-2.
  • Barman HN, Sheng Z, Fiaz S, Zhong M, Wu Y, Cai Y, Wang W, Jiao G, Tang S, Wei X, et al. Generation of a new thermo-sensitive genic male sterile rice line by targeted mutagenesis of TMS5 gene through CRISPR/Cas9 system. BMC Plant Biol. 2019;19(1):1–9. doi:10.1186/s12870-019-1715-0.
  • Shen C, Que Z, Xia Y, Tang N, Li D, He R, Cao M. Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol. 2017;60(6):539–47. doi:10.1007/s12374-016-0400-1.
  • Yu J, Miao J, Zhang Z, Xiong H, Zhu X, Sun X, Pan Y, Liang Y, Zhang Q, Abdul Rehman RM, et al. Alternative splicing of Os LG 3b controls grain length and yield in japonica rice. Plant Biotechnol J. 2018;16(9):1667–78. doi:10.1111/pbi.12903.
  • Xie Y, Niu B, Long Y, Li G, Tang J, Zhang Y, Ren D, Liu YG, Chen L. Suppression or knockout of SaF / SaM overcomes the Sa-mediated hybrid male sterility in rice. J Integr Plant Biol. 2017;59(9):669–79. doi:10.1111/jipb.12564.
  • Xie Y, Xu P, Huang J, Ma S, Xie X, Tao D, Chen L, Liu Y-G. Interspecific hybrid sterility in rice is mediated by OgTPR1 at the S1 locus encoding a peptidase-like protein. Mol Plant. 2017;10(8):1137–40. doi:10.1016/j.molp.2017.05.005.
  • Wang C, Liu Q, Shen Y, Hua Y, Wang J, Lin J, Wu M, Sun T, Cheng Z, Mercier R, et al. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol. 2019;37(3):283–86. doi:10.1038/s41587-018-0003-0.
  • Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature. 2019;565(7737):91–95. doi:10.1038/s41586-018-0785-8.
  • Østerberg JT, Xiang W, Olsen LI, Edenbrandt AK, Vedel SE, Christiansen A, Landes X, Andersen MM, Pagh P, Sandøe P, et al. Accelerating the domestication of new crops: feasibility and approaches. Trends Plant Sci. 2017;22(5):373–84. doi:10.1016/j.tplants.2017.01.004.
  • Fernie AR, Yan J. De Novo domestication: an alternative route toward new crops for the future. Mol Plant. 2019;12(5):615–31. doi:10.1016/j.molp.2019.03.016.
  • Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH, Weinl S, Freschi L, Voytas DF, Kudla J, Peres LEP. De Novo domestication of wild tomato using genome editing. Nat Biotechnol. 2018;36(12):1211–16. doi:10.1038/nbt.4272.
  • Lemmon ZH, Reem NT, Dalrymple J, Soyk S, Swartwood KE, Rodriguez-Leal D, Van Eck J, Lippman ZB. Rapid improvement of domestication traits in an orphan crop by genome editing. Nature Plants. 2018;4(10):766–70. doi:10.1038/s41477-018-0259-x.
  • Sedbrook JC, Phippen WB, Marks MD. New approaches to facilitate rapid domestication of a wild plant to an oilseed crop: example pennycress (Thlaspi arvense L.). Plant Sci. 2014;227:122–32. doi:10.1016/j.plantsci.2014.07.008.
  • Ivanizs L, Monostori I, Farkas A, Megyeri M, Mikó P, Türkösi E, Gaál E, Lenykó-Thegze A, Szőke-Pázsi K, Szakács É, et al. Unlocking the genetic diversity and population structure of a wild gene source of wheat, Aegilops biuncialis Vis., and its relationship with the heading time. Front Plant Sci. 2019;10:1531. doi:10.3389/fpls.2019.01531.
  • Pramanik D, Shelake RM, Kim MJ, Kim J-Y. CRISPR-mediated engineering across the central dogma in plant biology for basic research and crop improvement. Mol Plant. 2021;14(1):127–50. doi:10.1016/j.molp.2020.11.002.
  • González Guzmán M, Cellini F, Fotopoulos V, Balestrini R, Arbona V. New approaches to improve crop tolerance to biotic and abiotic stresses. Physiol Plant. 2022;174(1). doi:10.1111/ppl.13547.
  • Al-Sadi AM, Al-Moqbali HS, Al-Yahyai RA, Al-Said FA. AFLP data suggest a potential role for the low genetic diversity of acid lime (Citrus aurantifolia Swingle) in Oman in the outbreak of witches’ broom disease of lime. Euphytica. 2012;188(2):285–97. doi:10.1007/s10681-012-0728-7.
  • Collinge DB, Sarrocco S. Transgenic approaches for plant disease control: status and prospects 2021. null. 2022;71(1):207–25. doi:10.1111/ppa.13443.
  • Kettles GJ, Kanyuka K. Dissecting the molecular interactions between wheat and the fungal pathogen Zymoseptoria tritici. Front Plant Sci. 2016;7:508. doi:10.3389/fpls.2016.00508.
  • Tyagi S, Kumar R, Kumar V, Won SY, Shukla P. Engineering disease resistant plants through CRISPR-Cas9 technology. GM Crops & Food. 2021;12(1):125–44. doi:10.1080/21645698.2020.1831729.
  • Alphonse V, Marimuthu J, Murugan K. CRISPR/Cas system for the development of disease resistance in horticulture crops. CRISPR And RNAi Systems. 2021;107–28. Elsevier.
  • Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu Y-G, Zhao K. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLos One. 2016;11(4):e0154027. doi:10.1371/journal.pone.0154027.
  • Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom J-S, Huang S, Liu S, Vera Cruz C, Frommer WB, et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. The Plant Journal. 2015;82(4):632–43. doi:10.1111/tpj.12838.
  • Jia H, Zhang Y, Orbović V, Xu J, White FF, Jones JB, Wang N. Genome editing of the disease susceptibility gene Cs LOB 1 in citrus confers resistance to citrus canker. Plant Biotechnol J. 2017;15(7):817–23. doi:10.1111/pbi.12677.
  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu J-L, et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol. 2013;31(8):686–88. doi:10.1038/nbt.2650.
  • Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, et al. The CRISPR/C as 9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J. 2014;12(6):797–807. doi:10.1111/pbi.12200.
  • Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J-L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol. 2014;32(9):947–51. doi:10.1038/nbt.2969.
  • Zhang Y, Bai Y, Wu G, Zou S, Chen Y, Gao C, Tang D. Simultaneous modification of three homoeologs of Ta EDR 1 by genome editing enhances powdery mildew resistance in wheat. The Plant Journal. 2017;91(4):714–24. doi:10.1111/tpj.13599.
  • Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. . 2017;7(1):1–6. doi:10.1038/s41598-017-00578-x.
  • Ji X, Si X, Zhang Y, Zhang H, Zhang F, Gao C. Conferring DNA virus resistance with high specificity in plants using virus-inducible genome-editing system. Genome Biol. 2018;19(1):1–7. doi:10.1186/s13059-018-1580-4.
  • Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM. Crispr/cas9-mediated viral interference in plants. Genome Biol. 2015;16(1):1–11. doi:10.1186/s13059-015-0799-6.
  • Zaidi SS-E-A, Tashkandi M, Mansoor S, Mahfouz MM. Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front Plant Sci. 2016;7:1673.
  • Zhang T, Zheng Q, Yi X, An H, Zhao Y, Ma S, Zhou G. Establishing RNA virus resistance in plants by harnessing CRISPR immune system. Plant Biotechnol J. 2018;16(8):1415–23.
  • Farooq MU, Bashir MF, Khan M, Iqbal B, Ali Q. Role of crispr to improve abiotic stress tolerance in crop plants. Biol Clin Sci Res J. 2021;2021(1). doi:10.54112/bcsrj.v2021i1.69.
  • Kim D, Alptekin B, Budak H. CRISPR/Cas9 genome editing in wheat. Funct Integr Genomics. 2018;18(1):31–41. doi:10.1007/s10142-017-0572-x.
  • Yadav R, Thankappan R, Kumar A. Novel Approaches for Genome Editing to Develop Climate Smart Crops. Microbiomes And The Global Climate Change. 2021;267–91. Springer.
  • Raza A, Tabassum J, Fakhar AZ, Sharif R, Chen H, Zhang C, Ju L, Fotopoulos V, Siddique KHM, Singh RK, et al. Smart reprograming of plants against salinity stress using modern biotechnological tools. Crit Rev Biotechnol. 2022:1–28. doi:10.1080/07388551.2022.2093695
  • Raza A, Mubarik MS, Sharif R, Habib M, Jabeen W, Zhang C, Chen H, Chen Z-H, Siddique KHM, Zhuang W, et al. Developing drought‐smart, ready‐to‐grow future crops. Plant Genome. 2023;16(1):e20279. doi:10.1002/tpg2.20279.
  • Raza A, Charagh S, García-Caparrós P, Rahman MA, Ogwugwa VH, Saeed F, Jin W. Melatonin-mediated temperature stress tolerance in plants. GM Crops & Food. 2022;13(1):196–217. doi:10.1080/21645698.2022.2106111.
  • Raza A, Tabassum J, Kudapa H, Varshney RK. Can omics deliver temperature resilient ready-to-grow crops? Crit Rev Biotechnol. 2021;41(8):1209–32. doi:10.1080/07388551.2021.1898332.
  • Lou D, Wang H, Liang G, Yu D. OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci. 2017;8:993. doi:10.3389/fpls.2017.00993.
  • Li S, Chang L, Zhang J. Advancing organelle genome transformation and editing for crop improvement. Plant Commun. 2021;2(2):100141. doi:10.1016/j.xplc.2021.100141.
  • Okie JG, Smith VH, Martin-Cereceda M. Major evolutionary transitions of life, metabolic scaling and the number and size of mitochondria and chloroplasts. Proc R Soc B Biol Sci. 2016;283283(1831):20160611. doi:10.1098/rspb.2016.0611.
  • Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA. 2015;112(28):8529–36. doi:10.1073/pnas.1424031112.
  • Bacman SR, Williams SL, Pinto M, Peralta S, Moraes CT. Specific elimination of mutant mitochondrial genomes in patient-derived cells by mitoTalens. Nat Med. 2013;19(9):1111–13. doi:10.1038/nm.3261.
  • Kang B-C, Bae S-J, Lee S, Lee JS, Kim A, Lee H, Baek G, Seo H, Kim J, Kim J-S. Chloroplast and mitochondrial DNA editing in plants. Nat Plants. 2021;7(7):899–905. doi:10.1038/s41477-021-00943-9.
  • Lin C-P, Ko C-Y, Kuo C-I, Liu M-S, Schafleitner R, Chen LFO. Transcriptional slippage and RNA editing increase the diversity of transcripts in chloroplasts: insight from deep sequencing of Vigna radiata genome and transcriptome. PLos One. 2015;10(6):e0129396. doi:10.1371/journal.pone.0129396.
  • Gómez G, Pallás V, Zhang B. Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLos One. 2010;5(8):e12269. doi:10.1371/journal.pone.0012269.
  • Salvi S, Druka A, Milner SG, Gruszka, D. Induced genetic variation, TILLING and NGS-based cloning. Biotechnological Approaches To Barley Improvement. 2014;287–310. Springer.
  • Mushtaq M, Sakina A, Wani SH, Shikari AB, Tripathi P, Zaid A, Galla A, Abdelrahman M, Sharma M, Singh AK, et al. Harnessing genome editing techniques to engineer disease resistance in plants. Front Plant Sci. 2019;10:550. doi:10.3389/fpls.2019.00550.
  • Liang Z, Chen K, Zhang Y, Liu J, Yin K, Qiu J-L, Gao C. Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nat Protoc. 2018;13(3):413–30. doi:10.1038/nprot.2017.145.
  • Pineda M, Lear A, Collins JP, Kiani S. Safe CRISPR: challenges and possible solutions. Trends Biotechnol. 2019;37(4):389–401. doi:10.1016/j.tibtech.2018.09.010.
  • El-Mounadi K, Morales-Floriano ML, Garcia-Ruiz H. Principles, applications, and biosafety of plant genome editing using CRISPR-Cas9. Front Plant Sci. 2020;11:56. doi:10.3389/fpls.2020.00056.
  • Corrigan-Curay J, O’Reilly M, Kohn DB, Cannon PM, Bao G, Bushman FD, Carroll D, Cathomen T, Joung JK, Roth D, et al. Genome editing technologies: defining a path to clinic: genomic editing: establishing preclinical toxicology standards, bethesda, maryland 10 June 2014. Mol Ther. 2015;23(5):796–806. doi:10.1038/mt.2015.54.
  • Ma Y, Zhang L, Huang X. Genome modification by CRISPR/Cas9. FEBS J. 2014;281(23):5186–93. doi:10.1111/febs.13110.
  • National Academies of Sciences, Engineering and Medicine. Gene drives on the horizon: advancing science, navigating uncertainty, and aligning research with public values. Washington (DC): National Academies Press (US);2016. PMID: 27536751.
  • Woo JW, Kim J, Kwon SI, Corvalán C, Cho SW, Kim H, Kim S-G, Kim S-T, Choe S, Kim J-S. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol. 2015;33(11):1162–64. doi:10.1038/nbt.3389.
  • Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A. Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Commun. 2016;7(1):1–7. doi:10.1038/ncomms13274.
  • Subburaj S, Chung SJ, Lee C, Ryu S-M, Kim DH, Kim J-S, Bae S, Lee G-J. Site-directed mutagenesis in Petunia× hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep. 2016;35(7):1535–44. doi:10.1007/s00299-016-1937-7.
  • Murovec J, Guček K, Bohanec B, Avbelj M, Jerala R. DNA-free genome editing of Brassica oleracea and B. rapa protoplasts using CRISPR-Cas9 ribonucleoprotein complexes. Front Plant Sci. 2018;9:1594. doi:10.3389/fpls.2018.01594.
  • Mao Y, Zhang Z, Feng Z, Wei P, Zhang H, Botella JR, Zhu J-K. Development of germ‐line‐specific CRISPR‐Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol J. 2016;14(2):519–32. doi:10.1111/pbi.12468.
  • Molla KA, Yang Y. Crispr/cas-mediated base editing: technical considerations and practical applications. Trends Biotechnol. 2019;37(10):1121–42. doi:10.1016/j.tibtech.2019.03.008.
  • Chew WL, Tabebordbar M, Cheng JKW, Mali P, Wu EY, Ng AHM, Zhu K, Wagers AJ, Church GM. A multifunctional AAV–CRISPR–Cas9 and its host response. Nat Methods. 2016;13(10):868–74. doi:10.1038/nmeth.3993.
  • Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013;31(9):822–26. doi:10.1038/nbt.2623.
  • Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B. Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J. 2015;13(7):1002–10. doi:10.1111/pbi.12344.
  • Kleinstiver BP, Tsai SQ, Prew MS, Nguyen NT, Welch MM, Lopez JM, McCaw ZR, Aryee MJ, Joung JK. Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat Biotechnol. 2016;34(8):869–74. doi:10.1038/nbt.3620.
  • Leenay RT, Beisel CL. Deciphering, communicating, and engineering the CRISPR PAM. J Mol Biol. 2017;429(2):177–91. doi:10.1016/j.jmb.2016.11.024.
  • Wyvekens N, Topkar VV, Khayter C, Joung JK, Tsai SQ. Dimeric CRISPR RNA-guided FokI-dCas9 nucleases directed by truncated gRnas for highly specific genome editing. Hum Gene Ther. 2015;26(7):425–31. doi:10.1089/hum.2015.084.
  • O’Geen H, Abigail SY, Segal DJ. How specific is CRISPR/Cas9 really? Curr Opin Chem Biol. 2015;29:72–78.
  • Nakade S, Yamamoto T, Sakuma T. Cas9, Cpf1 and C2c1/2/3―What’s next? Bioengineered. 2017;8(3):265–73. doi:10.1080/21655979.2017.1282018.
  • Duensing N, Sprink T, Parrott WA, Fedorova M, Lema MA, Wolt JD, Bartsch D. Novel features and considerations for ERA and regulation of crops produced by genome editing. Frontiers In Bioengineering And Biotechnology. 2018;6:79.
  • Friedrichs S, Takasu Y, Kearns P, Dagallier B, Oshima R, Schofield J, Moreddu C. Meeting report of the OECD conference on “genome editing: applications in agriculture—implications for health, environment and regulation”. Springer; 2019.
  • Schiemann J, Robienski J, Schleissing S, Spök A, Sprink T, Wilhelm RA. Editorial: plant Genome Editing – Policies and Governance. Front Plant Sci. 2020;11:284. doi:10.3389/fpls.2020.00284.
  • Ammann K. Selected Innovative Solutions for the Regulation of GM Crops in Times of Gene Editing. Plant Biotechnology: Progress In Genomic Era. 2019;3–41. Springer.
  • Wolt JD, Wang K, Yang B. The regulatory status of genome‐edited crops. Plant Biotechnol J. 2016;14(2):510–18. doi:10.1111/pbi.12444.
  • Wolt JD, Wolf C. Policy and governance perspectives for regulation of genome edited crops in the United States. Front Plant Sci. 2018;9:1606. doi:10.3389/fpls.2018.01606.
  • Kok EJ, Glandorf DCM, Prins TW, Visser RGF. Food and environmental safety assessment of new plant varieties after the European Court decision: process-triggered or product-based? Trends in Food Sci Technol. 2019;88:24–32. doi:10.1016/j.tifs.2019.03.007.
  • Okoli AS, Blix T, Myhr AI, Xu W, Xu X. Sustainable use of CRISPR/Cas in fish aquaculture: the biosafety perspective. Transgenic Res. 2021;31(1):1–21. doi:10.1007/s11248-021-00274-7.
  • Eckerstorfer MF, Engelhard M, Heissenberger A, Simon S, Teichmann H. Plants developed by new genetic modification techniques—comparison of existing regulatory frameworks in the EU and non-EU countries. Front Bioeng Biotechnol. 2019;7:26. doi:10.3389/fbioe.2019.00026.
  • Kupferschmidt K. EU verdict on CRISPR crops dismays scientists. Washington, DC, USA: American Association for the Advancement of Science; 2018. doi:10.1126/science.361.6401.435.
  • Tuteja N, Verma S, Sahoo RK, Raveendar S, Reddy IBL. Recent advances in development of marker-free transgenic plants: regulation and biosafety concern. J Biosci. 2012;37(1):167–97. doi:10.1007/s12038-012-9187-5.
  • Greer SL, Trump B. Regulation and regime: the comparative politics of adaptive regulation in synthetic biology. Policy Sci. 2019;52(4):505–24. doi:10.1007/s11077-019-09356-0.
  • Molinari HBC, Silva N, Prado G, Lopes Filho J.V, Vieira L, Hugo Bruno Correa Molinari CNPAE, Letícia RV, Silva NVE, Prado GS, Lopes Filho JH. CRISPR technology in plant genome editing: biotechnology applied to agriculture. Embrapa Agroenergia-Livro científico (ALICE). 2021.
  • Waltz E. CRISPR-edited crops free to enter market, skip regulation. Nat Biotechnol. 2016;34(6):582–582. doi:10.1038/nbt0616-582.
  • Davison J, Ammann K. New GMO regulations for old: determining a new future for EU crop biotechnology. GM Crops & Food. 2017;8(1):13–34. doi:10.1080/21645698.2017.1289305.
  • Arpaia S, Birch ANE, Kiss J, van Loon JJA, Messéan A, Nuti M, Perry JN, Sweet JB, Tebbe CC. Assessing environmental impacts of genetically modified plants on non-target organisms: the relevance of in planta studies. Sci Total Environ. 2017;583:123–32. doi:10.1016/j.scitotenv.2017.01.039.
  • Whelan AI, Lema MA. Regulatory framework for gene editing and other new breeding techniques (NBTs) in Argentina. GM Crops & Food. 2015;6(4):253–65. doi:10.1080/21645698.2015.1114698.
  • Callaway E. CRISPR plants now subject to tough GM laws in European Union. Nature. 2018;560(7716):16–17. doi:10.1038/d41586-018-05814-6.
  • Kumar A. Application, Regulation, Ethical Concerns and Governance of Genome-Editing Technologies: an Overview. Asian Biotechnology & Development Review. 2019;21.
  • Menz J, et al. Genome edited crops touch the market: a view on the global development and regulatory environment. Front Plant Sci. 2020;21: p 11.
  • Jaffe G. The regulation of genome-edited crops, in Genome editing for precision crop breeding. Tylor & Francis, UK, London: Burleigh Dodds Science Publishing; 2021. pp. 279–321.
  • Zhang D, Zhang Z, Unver T, Zhang B. CRISPR/Cas: a powerful tool for gene function study and crop improvement. J Adv Res. 2021;29:207–21. doi:10.1016/j.jare.2020.10.003.
  • Tussipkan D, Manabayeva SA. Employing CRISPR/Cas Technology for the Improvement of Potato and Other Tuber Crops. Front Plant Sci. 2021;12:12. doi:10.3389/fpls.2021.747476.
  • Hahn F, Nekrasov V. CRISPR/Cas precision: do we need to worry about off-targeting in plants? Plant Cell Rep. 2019;38(4):437–41. doi:10.1007/s00299-018-2355-9.
  • Macovei A, Sevilla NR, Cantos C, Jonson GB, Slamet‐Loedin I, Čermák T, Voytas DF, Choi I-R, Chadha‐Mohanty P. Novel alleles of rice eIF4G generated by CRISPR/Cas9‐targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnol J. 2018;16(11):1918–27. doi:10.1111/pbi.12927.
  • Alqahantani N, Alotaibi B, Alshumrani R, Bamhrez M, Unver T, Tombuloglu H. CRISPR Applications in Crops. Oil Crop Genomics. 2021;367–81. Springer.
  • Ortigosa A, Gimenez-Ibanez S, Leonhardt N, Solano R. Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnol J. 2019;17(3):665–73. doi:10.1111/pbi.13006.
  • Zhang Z, Ge X, Luo X, Wang P, Fan Q, Hu G, Xiao J, Li F, Wu J. Simultaneous editing of two copies of Gh14-3-3d confers enhanced transgene-clean plant defense against Verticillium dahliae in allotetraploid upland cotton. Front Plant Sci. 2018;9:842. doi:10.3389/fpls.2018.00842.
  • Li R, Liu C, Zhao R, Wang L, Chen L, Yu W, Zhang S, Sheng J, Shen L. Crispr/cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol. 2019;19(1):1–13. doi:10.1186/s12870-018-1627-4.
  • Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A. Development of broad virus resistance in non‐transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol. 2016;17(7):1140–53. doi:10.1111/mpp.12375.
  • Zaman Q U, Raza A, Gill R Ali, Hussain M Azhar, Wang H Feng and Varshney R K. 2023. New possibilities for trait improvement via mobile CRISPR-RNA. Trends Biotechnol.2023. doi: 10.1016/j.tibtech.2023.05.001.

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