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Review Article

Evidence and opportunities for developing non-transgenic genome edited crops using site-directed nuclease 1 approach

, , , , , , , & show all
Received 04 Feb 2022, Accepted 18 Sep 2023, Published online: 01 Nov 2023

References

  • Greene EA, Codomo CA, Taylor NE, et al. Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics. 2003;164:731–740. doi: 10.1093/genetics/164.2.731.
  • McCallum CM, Comai L, Greene EA, et al. Targeted screening for induced mutations. Nat Biotechnol. 2000;18:455–457. doi: 10.1038/74542.
  • Tadele Z, Mba C, Till BJ. TILLING for mutations in model plants and crops. In: Jain SM, Brar DS, editors. Molecular techniques in crop improvement. Dordrecht: Springer Netherlands; 2010. p. 307–332. doi: 10.1007/978-90-481-2967-6_13.
  • Mamrutha HM, Kumar R, Venkatesh K, et al. Genetic transformation of wheat – present status and future potential. J Wheat Res. 2014;6:107–119.
  • Kumar R, Kaur A, Pandey A, et al. CRISPR-based genome editing in wheat: a comprehensive review and future prospects. Mol Biol Rep. 2019;46:3557–3569. doi: 10.1007/s11033-019-04761-3.
  • Jackson AL, Linsley PS. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat Rev Drug Discov. 2010;9:57–67. doi: 10.1038/nrd3010.
  • Travella S, Klimm TE, Keller B. RNA interference-based gene silencing as an efficient tool for functional genomics in hexaploid bread wheat. Plant Physiol. 2006;142:6–20. doi: 10.1104/pp.106.084517.
  • Mamrutha HM, Kumar R, Wadhwa Z, et al. A improving grain weight in wheat through CRISPR/Cas9 mediated genome editing. Wheat Barley News Lett. 2020;13:2.
  • Abdallah NA, Prakash CS, McHughen AG. Genome editing for crop improvement: challenges and opportunities. GM Crops Food. 2015;6:183–205. doi: 10.1080/21645698.2015.1129937.
  • Kamburova VS, Nikitina EV, Shermatov SE, et al. Genome editing in plants: an overview of tools and applications. Int J Agron. 2017;2017:1–15. doi: 10.1155/2017/7315351.
  • Zhu X, Qi T, Yang Q, et al. Host-induced gene silencing of the MAPKK gene PsFUZ7 confers stable resistance to wheat stripe rust. Plant Physiol. 2017;175:1853–1863. doi: 10.1104/pp.17.01223.
  • Zaidi SS-A, Vanderschuren H, Qaim M, et al. New plant breeding technologies for food security. Science. 2019;363:1390–1391. doi: 10.1126/science.aav6316.
  • Arpaia S, Birch ANE, Chesson A, et al. Scientific opinion addressing the safety assessment of plants developed using zinc finger nuclease 3 and other site-directed nucleases with similar function. EFSA J. 2012;10(10):2943.
  • van de Wiel CCM, Schaart JG, Lotz LAP, et al. New traits in crops produced by genome editing techniques based on deletions. Plant Biotechnol Rep. 2017;11:1–8. doi: 10.1007/s11816-017-0425-z.
  • Matres JM, Hilscher J, Datta A, et al. Genome editing in cereal crops: an overview. Transgenic Res. 2021;30:461–498. doi: 10.1007/s11248-021-00259-6.
  • Wang Y, Cheng X, Shan Q, et al. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol. 2014;32:947–951. doi: 10.1038/nbt.2969.
  • Abe F, Haque E, Hisano H, et al. Genome-edited triple-recessive mutation alters seed dormancy in wheat. Cell Rep. 2019;28:1362–1369.e4. doi: 10.1016/j.celrep.2019.06.090.
  • Zhang A, Liu Y, Wang F, et al. Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol Breed. 2019;39:47. doi: 10.1007/s11032-019-0954-y.
  • Okada A, Arndell T, Borisjuk N, et al. CRISPR/Cas9-mediated knockout of Ms1 enables the rapid generation of male-sterile hexaploid wheat lines for use in hybrid seed production. Plant Biotechnol J. 2019;17:1905–1913. doi: 10.1111/pbi.13106.
  • Sánchez-León S, Gil-Humanes J, Ozuna CV, et al. Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J. 2018;16:902–910. doi: 10.1111/pbi.12837.
  • Singh M, Kumar M, Albertsen MC, et al. 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;97:371–383. doi: 10.1007/s11103-018-0749-2.
  • Brauer EK, Balcerzak M, Rocheleau H, et al. Genome editing of a deoxynivalenol-induced transcription factor confers resistance to Fusarium graminearum in wheat. Mol Plant Microbe Interact. 2020;33:553–560. doi: 10.1094/MPMI-11-19-0332-R.
  • Clasen BM, Stoddard TJ, Luo S, et al. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J. 2016;14:169–176. doi: 10.1111/pbi.12370.
  • Veillet F, Perrot L, Chauvin L, et al. Transgene-free genome editing in tomato and potato plants using Agrobacterium-mediated delivery of a CRISPR/Cas9 cytidine base editor. Int J Mol Sci. 2019;20:402. doi: 10.3390/ijms20020402.
  • Haun W, Coffman A, Clasen BM, et al. Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J. 2014;12:934–940. doi: 10.1111/pbi.12201.
  • Shan Q, Zhang Y, Chen K, et al. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J. 2015;13:791–800. doi: 10.1111/pbi.12312.
  • Li M, Li X, Zhou Z, et al. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci. 2016;7:377. doi: 10.3389/fpls.2016.00377.
  • Wang F, Wang C, Liu P, et al. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLOS One. 2016;11:e0154027. doi: 10.1371/journal.pone.0154027.
  • Tang L, Mao B, Li Y, et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep. 2017;7:14438. doi: 10.1038/s41598-017-14832-9.
  • Zhou H, He M, Li J, et al. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep. 2016;6:37395. doi: 10.1038/srep37395.
  • Kim Y-A, Moon H, Park C-J. CRISPR/Cas9-targeted mutagenesis of Os8N3 in rice to confer resistance to Xanthomonas oryzae pv. oryzae. Rice. 2019;12:67. doi: 10.1186/s12284-019-0325-7.
  • Sheng X, Sun Z, Wang X, et al. Improvement of the rice “easy-to-shatter” trait via CRISPR/Cas9-mediated mutagenesis of the qSH1 gene. Front Plant Sci. 2020;11:619. doi: 10.3389/fpls.2020.00619.
  • Liao S, Qin X, Luo L, et al. CRISPR/Cas9-induced mutagenesis of semi-rolled leaf1, 2 confers curled leaf phenotype and drought tolerance by influencing protein expression patterns and ROS scavenging in rice (Oryza sativa L.). Agronomy. 2019;9:728. doi: 10.3390/agronomy9110728.
  • Wang F, Han T, Song Q, et al. The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell. 2020;32(10):3124–3138. doi: 10.1105/tpc.20.00289.
  • Zhou J, Peng Z, Long J, et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J. 2015;82:632–643. doi: 10.1111/tpj.12838.
  • Macovei A, Sevilla NR, Cantos C, et al. Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnol. 2018;16(11):1918–1927.
  • Santosh Kumar VV, Verma RK, Yadav SK, et al. CRISPR–Cas9 mediated genome editing of drought and salt tolerance (OsDST) gene in indica mega rice cultivar MTU1010. Physiol Mol Biol Plants. 2020;26:1099–1110. doi: 10.1007/s12298-020-00819-w.
  • Yin X, Anand A, Quick P, et al. Editing a stomatal developmental gene in rice with CRISPR/Cpf1. In: Qi Y, editor. Plant genome editing with CRISPR systems. Methods and protocols. New York, NY: Springer; 2019. p. 257–268.
  • Yin X, Biswal AK, Dionora J, et al. CRISPR–Cas9 and CRISPR–Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep. 2017;36:745–757. doi: 10.1007/s00299-017-2118-z.
  • Baysal C, He W, Drapal M, et al. Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming. Proc Natl Acad Sci U S A. 2020;117:26503–26512. doi: 10.1073/pnas.2014860117.
  • Pérez L, Soto E, Farré G, et al. CRISPR/Cas9 mutations in the rice Waxy/GBSSI gene induce allele-specific and zygosity-dependent feedback effects on endosperm starch biosynthesis. Plant Cell Rep. 2019;38:417–433. doi: 10.1007/s00299-019-02388-z.
  • Khan MSS, Basnet R, Islam SA, et al. Mutational analysis of OsPLDα1 reveals its involvement in phytic acid biosynthesis in rice grains. J Agric Food Chem. 2019;67:11436–11443. doi: 10.1021/acs.jafc.9b05052.
  • Jiang J, Zhao J, Duan W, et al. TaAMT2;3a, a wheat AMT2-type ammonium transporter, facilitates the infection of stripe rust fungus on wheat. BMC Plant Biol. 2019;19:239. doi: 10.1186/s12870-019-1841-8.
  • Jiang M, Liu Y, Liu Y, et al. Mutation of inositol 1,3,4-trisphosphate 5/6-kinase6 impairs plant growth and phytic acid synthesis in rice. Plants. 2019;8:114. doi: 10.3390/plants8050114.
  • Akama K, Akter N, Endo H, et al. An in vivo targeted deletion of the calmodulin-binding domain from rice glutamate decarboxylase 3 (OsGAD3) increases γ-aminobutyric acid content in grains. Rice. 2020;13:20. doi: 10.1186/s12284-020-00380-w.
  • Li T, Liu B, Spalding MH, et al. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol. 2012;30:390–392. doi: 10.1038/nbt.2199.
  • Shan Q, Wang Y, Li J, et al. Targeted genome modification of crop plants using a CRISPR–Cas system. Nat Biotechnol. 2013;31:686–688. doi: 10.1038/nbt.2650.
  • Mao C, He J, Liu L, et al. OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol J. 2020;18(2):429–442. doi: 10.1111/pbi.13209.
  • Li C, Liu C, Qi X, et al. RNA-guided Cas9 as an in vivo desired-target mutator in maize. Plant Biotechnol J. 2017;15:1566–1576. doi: 10.1111/pbi.12739.
  • Bage SA, Barten TJ, Brown AN, et al. Genetic characterization of novel and CRISPR–Cas9 gene edited maize brachytic 2 alleles. Plant Gene. 2020;21:100198. doi: 10.1016/j.plgene.2019.100198.
  • Xie K, Wu S, Li Z, et al. Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase. Theor Appl Genet. 2018;131:1363–1378. doi: 10.1007/s00122-018-3083-9.
  • Aggarwal S, Kumar A, Bhati KK, et al. RNAi-mediated downregulation of inositol pentakisphosphate kinase (IPK1) in wheat grains decreases phytic acid levels and increases Fe and Zn accumulation. Front Plant Sci. 2018;9:259. doi: 10.3389/fpls.2018.00259.
  • Regina A, Bird A, Topping D, et al. High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc Natl Acad Sci U S A. 2006;103:3546–3551. doi: 10.1073/pnas.0510737103.
  • Loukoianov A, Yan L, Blechl A, et al. Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol. 2005;138:2364–2373. doi: 10.1104/pp.105.064287.
  • Yan L, Loukoianov A, Blechl A, et al. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science. 2004;303:1640–1644. doi: 10.1126/science.1094305.
  • Gasparis S, Orczyk W, Zalewski W, et al. The RNA-mediated silencing of one of the Pin genes in allohexaploid wheat simultaneously decreases the expression of the other, and increases grain hardness. J Exp Bot. 2011;62:4025–4036. doi: 10.1093/jxb/err103.
  • Zhao B, Wu TT, Ma SS, et al. TaD27-B gene controls the tiller number in hexaploid wheat. Plant Biotechnol J. 2020;18:513–525. doi: 10.1111/pbi.13220.
  • Ouyang X, Hong X, Zhao X, et al. Knock out of the PHOSPHATE 2 gene TaPHO2-A1 improves phosphorus uptake and grain yield under low phosphorus conditions in common wheat. Sci Rep. 2016;6:29850. doi: 10.1038/srep29850.
  • Sestili F, Pagliarello R, Zega A, et al. Enhancing grain size in durum wheat using RNAi to knockdown GW2 genes. Theor Appl Genet. 2019;132:419–429. doi: 10.1007/s00122-018-3229-9.
  • Sakuma S, Golan G, Guo Z, et al. Unleashing floret fertility in wheat through the mutation of a homeobox gene. Proc Natl Acad Sci U S A. 2019;116:5182–5187. doi: 10.1073/pnas.1815465116.
  • Qi T, Zhu X, Tan C, et al. Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnol J. 2018;16:797–807. doi: 10.1111/pbi.12829.
  • Rupp JS, Cruz L, Trick HN, et al. RNAi-mediated silencing of endogenous wheat genes EIF(Iso)4E-2 and EIF4G induce resistance to multiple RNA viruses in transgenic wheat. Crop Sci. 2019;59:2642–2651. doi: 10.2135/cropsci2018.08.0518.
  • Liu H, Li H, Hao C, et al. TaDA1, a conserved negative regulator of kernel size, has an additive effect with TaGW2 in common wheat (Triticum aestivum L.). Plant Biotechnol J. 2020;18:1330–1342. doi: 10.1111/pbi.13298.
  • Chen W, Kastner C, Nowara D, et al. Host-induced silencing of Fusarium culmorum genes protects wheat from infection. J Exp Bot. 2016;67:4979–4991. doi: 10.1093/jxb/erw263.
  • Zhao Y, Sui X, Xu L, et al. Plant-mediated RNAi of grain aphid CHS1 gene confers common wheat resistance against aphids: RNAi of grain aphid CHS1. Pest Manag Sci. 2018;74:2754–2760. doi: 10.1002/ps.5062.
  • Panwar V, Jordan M, McCallum B, et al. Host-induced silencing of essential genes in Puccinia triticina through transgenic expression of RNAi sequences reduces severity of leaf rust infection in wheat. Plant Biotechnol J. 2018;16:1013–1023. doi: 10.1111/pbi.12845.
  • Yang J, Wang M, Li W, et al. Reducing expression of a nitrate-responsive bZIP transcription factor increases grain yield and N use in wheat. Plant Biotechnol J. 2019;17:1823–1833. doi: 10.1111/pbi.13103.
  • Wang X, Zhi P, Fan Q, et al. Wheat CHD3 protein TaCHR729 regulates the cuticular wax biosynthesis required for stimulating germination of Blumeria graminis f.sp. tritici. J Exp Bot. 2019;70:701–713. doi: 10.1093/jxb/ery377.
  • Huai B, Yang Q, Qian Y, et al. ABA-induced sugar transporter TaSTP6 promotes wheat susceptibility to stripe rust. Plant Physiol. 2019;181:1328–1343. doi: 10.1104/pp.19.00632.
  • Hazard B, Zhang X, Colasuonno P, et al. Induced mutations in the starch branching enzyme II (SBEII) genes increase amylose and resistant starch content in durum wheat. Crop Sci. 2012;52:1754–1766. doi: 10.2135/cropsci2012.02.0126.
  • Bovina R, Brunazzi A, Gasparini G, et al. Development of a TILLING resource in durum wheat for reverse- and forward-genetic analyses. Crop Pasture Sci. 2014;65:112. doi: 10.1071/CP13226.
  • Dong C, Dalton-Morgan J, Vincent K, et al. A modified TILLING method for wheat breeding. Plant Genome. 2009;2:39–47. doi: 10.3835/plantgenome2008.10.0012.
  • Fang H, Meng Q, Xu J, et al. Knock-down of stress inducible OsSRFP1 encoding an E3 ubiquitin ligase with transcriptional activation activity confers abiotic stress tolerance through enhancing antioxidant protection in rice. Plant Mol Biol. 2015;87:441–458. doi: 10.1007/s11103-015-0294-1.
  • Guo M, Wang R, Wang J, et al. ALT1, a Snf2 family chromatin remodeling ATPase, negatively regulates alkaline tolerance through enhanced defense against oxidative stress in rice. PLOS One. 2014;9:e112515. doi: 10.1371/journal.pone.0112515.
  • Lu K, Wu B, Wang J, et al. Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol J. 2018;16:1710–1722. doi: 10.1111/pbi.12907.
  • Ning Y, Jantasuriyarat C, Zhao Q, et al. The SINA E3 ligase OsDIS1 negatively regulates drought response in rice. Plant Physiol. 2011;157:242–255. doi: 10.1104/pp.111.180893.
  • Li D, Liu H, Yang Y, et al. Down-regulated expression of RACK1 gene by RNA interference enhances drought tolerance in rice. Rice Sci. 2009;16:14–20. doi: 10.1016/S1672-6308(08)60051-7.
  • Ko MR, Song M-H, Kim JK, et al. RNAi-mediated suppression of three carotenoid-cleavage dioxygenase genes, OsCCD1, 4a, and 4b, increases carotenoid content in rice. J Exp Bot. 2018;69:5105–5116. doi: 10.1093/jxb/ery300.
  • Xie Y, Niu B, Long Y, et al. Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice. J Integr Plant Biol. 2017;59:669–679. doi: 10.1111/jipb.12564.
  • Marko D, El-Shershaby A, Carriero F, et al. Identification and characterization of a thermotolerant TILLING allele of heat shock binding protein 1 in tomato. Genes. 2019;10:516. doi: 10.3390/genes10070516.
  • Gauffier C, Lebaron C, Moretti A, et al. A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy. Plant J. 2016;85:717–729. doi: 10.1111/tpj.13136.
  • Mazzucato A, Cellini F, Bouzayen M, et al. A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. Mol Breed. 2015;35:22. doi: 10.1007/s11032-015-0222-8.
  • Knoll JE, Ramos ML, Zeng Y, et al. TILLING for allergen reduction and improvement of quality traits in peanut (Arachis hypogaea L.). BMC Plant Biol. 2011;11:81. doi: 10.1186/1471-2229-11-81.
  • Sabetta W, Alba V, Blanco A, et al. sunTILL: a TILLING resource for gene function analysis in sunflower. Plant Methods. 2011;7:20. doi: 10.1186/1746-4811-7-20.
  • Dahmani-Mardas F, Troadec C, Boualem A, et al. Engineering melon plants with improved fruit shelf life using the TILLING approach. PLOS One. 2010;5:e15776. doi: 10.1371/journal.pone.0015776.
  • Chawade A, Sikora P, Bräutigam M, et al. Development and characterization of an oat TILLING-population and identification of mutations in lignin and β-glucan biosynthesis genes. BMC Plant Biol. 2010;10:86. doi: 10.1186/1471-2229-10-86.
  • Nekrasov V, Wang C, Win J, et al. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep. 2017;7:482. doi: 10.1038/s41598-017-00578-x.
  • Mao Y, Botella JR, Liu Y, et al. Gene editing in plants: progress and challenges. Natl Sci Rev. 2019;6:421–437. doi: 10.1093/nsr/nwz005.
  • Aliaga-Franco N, Zhang C, Presa S, et al. Identification of transgene-free CRISPR-edited plants of rice, tomato, and Arabidopsis by monitoring DsRED fluorescence in dry seeds. Front Plant Sci. 2019;10:1150. doi: 10.3389/fpls.2019.01150.
  • Xu R-F, Li H, Qin R-Y, et al. Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep. 2015;5:11491. doi: 10.1038/srep11491.
  • Jung YJ, Lee HJ, Kim JH, et al. CRISPR/Cas9-targeted mutagenesis of F3′ H, DFR and LDOX, genes related to anthocyanin biosynthesis in black rice (Oryza sativa L.). Plant Biotechnol Rep. 2019;13:521–531. doi: 10.1007/s11816-019-00579-4.
  • Zhang Y, Liang Z, Zong Y, et al. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun. 2016;7:12617. doi: 10.1038/ncomms12617.
  • Liang Z, Chen K, Li T, et al. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun. 2017;8:14261. doi: 10.1038/ncomms14261.
  • Chandrasekaran J, Brumin M, Wolf D, et al. Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology: virus resistance in cucumber using CRISPR/Cas9. Mol Plant Pathol. 2016;17:1140–1153. doi: 10.1111/mpp.12375.
  • Hu B, Li D, Liu X, et al. Engineering non-transgenic gynoecious cucumber using an improved transformation protocol and optimized CRISPR/Cas9 system. Mol Plant. 2017;10:1575–1578. doi: 10.1016/j.molp.2017.09.005.
  • Malnoy M, Viola R, Jung M-H, et al. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci. 2016;7:1904.
  • Chen R, Xu Q, Liu Y, et al. Generation of transgene-free maize male sterile lines using the CRISPR/Cas9 system. Front Plant Sci. 2018;9:1180. doi: 10.3389/fpls.2018.01180.
  • Zhang J, Zhang X, Chen R, et al. Generation of transgene-free semidwarf maize plants by gene editing of gibberellin-oxidase20-3 using CRISPR/Cas9. Front Plant Sci. 2020;11:1048. doi: 10.3389/fpls.2020.01048.
  • Gupta S, Kumar A, Patel R, et al. Genetically modified crop regulations: scope and opportunity using the CRISPR–Cas9 genome editing approach. Mol Biol Rep. 2021;48:4851–4863. doi: 10.1007/s11033-021-06477-9.
  • Schmidt SM, Belisle M, Frommer WB. The evolving landscape around genome editing in agriculture: many countries have exempted or move to exempt forms of genome editing from GMO regulation of crop plants. EMBO Rep. 2020;21:e50680. doi: 10.15252/embr.202050680.
  • Dobrovidova O. Russia joins in global gene-editing bonanza. Nature. 2019;569:319–320. doi: 10.1038/d41586-019-01519-6.
  • Safety Assessment of Genome Edited Plants. Office Memorandum, F. No. C-12013/3/2020-CS-III dated 30.03.2022. MoEFCC; 2022.
  • Waltz E. Gene-edited CRISPR mushroom escapes US regulation. Nature. 2016;532:293–293. doi: 10.1038/nature.2016.19754.
  • Lemmon ZH, Reem NT, Dalrymple J, et al. Rapid improvement of domestication traits in an orphan crop by genome editing. Nat Plants. 2018;4:766–770. doi: 10.1038/s41477-018-0259-x.
  • Zsögön A, Čermák T, Naves ER, et al. De novo domestication of wild tomato using genome editing. Nat Biotechnol. 2018;36:1211–1216. doi: 10.1038/nbt.4272.
  • Metje-Sprink J, Sprink T, Hartung F. Genome-edited plants in the field. Curr Opin Biotechnol. 2020;61:1–6. doi: 10.1016/j.copbio.2019.08.007.

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