Abstract
Plant breeding is well recognized as one of the most important means to meet food security challenges caused by the ever-increasing world population. During the past three decades, plant breeding has been empowered by both new knowledge on trait development and regulation (e.g., functional genomics) and new technologies (e.g., biotechnologies and phenomics). Gene editing, particularly by clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas) and its variants, has become a powerful technology in plant research and may become a game-changer in plant breeding. Traits are conferred by coding and non-coding genes. From this perspective, we propose different editing strategies for these two types of genes. The activity of an encoded enzyme and its quantity are regulated at transcriptional and post-transcriptional, as well as translational and post-translational, levels. Different strategies are proposed to intervene to generate gene functional variations and consequently phenotype changes. For non-coding genes, trait modification could be achieved by regulating transcription of their own or target genes via gene editing. Also included is a scheme of protoplast editing to make gene editing more applicable in plant breeding. In summary, this review provides breeders with a host of options to translate gene biology into practical breeding strategies, i.e., to use gene editing as a mechanism to commercialize gene biology in plant breeding.
概要
人口不断增长给世界粮食安全带来了严峻的挑 战,植物育种是应对这一挑战的最重要手段之 一。过去三十年来,性状形成和调控的新知识(如 功能基因组学)和新技术(如生物信息学和表型 组学)极大地支持了植物育种的发展。基因编辑, 特别是基于CRISPR/Cas 技术和其衍生技术,已 成为强有力的植物研究技术,可能直接改变植物 育种的方法和策略。植物表型性状受编码基因和 非编码基因的控制,在本文中,我们提出了编辑 这两类基因的不同策略。对于编码基因,其编码 蛋白的活性和数量可在转录和转录后水平以及 翻译和翻译后水平加以调节,我们由此提出了创 造基因功能性变异从而改变性状表型的基因编 辑策略。对于非编码基因,则可以采用基因编辑 技术对其转录水平或对靶基因的目标序列加以 改造,达到产生新的性状的目的。此外,我们还 提出了一种基于原生质体的基因编辑方案,使基 因编辑技术更适合于植物育种。总之,本文提出 了一系列可供植物育种者选择的将基因生物学 知识转化为实用育种策略的方案,即基因编辑技 术成为将基因生物学知识用于植物育种的技术。
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References
Al-Zeer MA, Dutkiewicz M, von Hacht A, et al., 2019. Alternatively spliced variants of the 5'-UTR of the ARPC2 mRNA regulate translation by an internal ribosome entry site (IRES) harboring a guanine-quadruplex motif. RNA Biol, 16(11):1622–1632. https://doi.org/10.1080/15476286.2019.1652524
Apitz J, Nishimura K, Schmied J, et al., 2016. Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol, 170(4):2040–2051. https://doi.org/10.1104/pp.15.01945
Beale SI, 1999. Enzymes of chlorophyll biosynthesis. Photosynth Res, 60(1):43–73. https://doi.org/10.1023/a:1006297731456
Butelli E, Licciardello C, Zhang Y, et al., 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 24(3): 1242–1255. https://doi.org/10.1105/tpc.111.095232
Cermak T, Doyle EL, Christian M, et al., 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res, 39(12):e82. https://doi.org/10.1093/nar/gkr218
Čermák T, Baltes NJ, Čegan R, et al., 2015. High-frequency, precise modification of the tomato genome. Genome Biol, 16:232. https://doi.org/10.1186/s13059-015-0796-9
Chavez A, Scheiman J, Vora S, et al., 2015. Highly efficient Cas9-mediated transcriptional programming. Nat Methods, 12(4):326–328. https://doi.org/10.1038/nmeth.3312
Chen KL, Wang YP, Zhang R, et al., 2019. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol, 70:667–697. https://doi.org/10.1146/annurev-arplant-050718-100049
Czarnecki O, Hedtke B, Melzer M, et al., 2011. An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell, 23(12):4476–4491. https://doi.org/10.1105/tpc.111.086421
Deng X, Cao XF, 2017. Roles of pre-mRNA splicing and polyadenylation in plant development. Curr Opin Plant Biol, 35:45–53. https://doi.org/10.1016/j.pbi.2016.11.003
Deribe YL, Pawson T, Dikic I, 2010. Post-translational modifications in signal integration. Nat Struct Mol Biol, 17(6): 666–672. https://doi.org/10.1038/nsmb.1842
Duan GY, Walther D, 2015. The roles of post-translational modifications in the context of protein interaction networks. PLoS Comput Biol, 11(2):e1004049. https://doi.org/10.1371/journal.pcbi.1004049
Endo A, Masafumi M, Kaya H, et al., 2016. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci Rep, 6:38169. https://doi.org/10.1038/srep38169
Eş I, Gavahian M, Marti-Quijal FJ, et al., 2019. The application of the CRISPR-Cas9 genome editing machinery in food and agricultural science: current status, future perspectives, and associated challenges. Biotechnol Adv, 37(3):410–421. https://doi.org/10.1016/j.biotechadv.2019.02.006
Espley RV, Brendolise C, Chagné D, et al., 2009. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell, 21(1):168–183. https://doi.org/10.1105/tpc.108.059329
Filichkin S, Priest HD, Megraw M, et al., 2015. Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress. Curr Opin Plant Biol, 24:125–135. https://doi.org/10.1016/j.pbi.2015.02.008
Fossi M, Amundson K, Kuppu S, et al., 2019. Regeneration of Solanum tuberosum plants from protoplasts induces widespread genome instability. Plant Physiol, 180:78–86. https://doi.org/10.1104/pp.18.00906
Goslings D, Meskauskiene R, Kim C, et al., 2004. Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J, 40(6):957–967. https://doi.org/10.1111/j.1365-313x.2004.02262.x
Hickey LT, Hafeez AN, Robinson H, et al., 2019. Breeding crops to feed 10 billion. Nat Biotechnol, 37(2):744–754. https://doi.org/10.1038/s41587-019-0152-9
Hu JH, Miller SM, Geurts MH, et al., 2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature, 556(7699):57–63. https://doi.org/10.1038/nature26155
Hua K, Tao XP, Zhu JK, 2018. Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J, 17(2):499–504. https://doi.org/10.1111/pbi.12993
Hua K, Zhang JS, Botella JR, et al., 2019. Perspectives on the application of genome-editing technologies in crop breeding. Mol Plant, 12(8):1047–1059. https://doi.org/10.1016/j.molp.2019.06.009
Huber SC, Hardin SC, 2004. Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Curr Opin Plant Biol, 7(3):318–322. https://doi.org/10.1016/j.pbi.2004.03.002
Hunt AG, 2014. The Arabidopsis polyadenylation factor subunit CPSF30 as conceptual link between mRNA polyadenylation and cellular signaling. Curr Opin Plant Biol, 21: 128–132. https://doi.org/10.1016/j.pbi.2014.07.002
Jia HG, Zhang YZ, Orbović V, et al., 2017. Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J, 15(7):817–823. https://doi.org/10.1111/pbi.12677
Jiang M, Liu YH, Li RQ, et al., 2019. A suppressor mutation partially reverts the xantha trait via lowered methylation in the promoter of genomes uncoupled 4 in Rice. Front Plant Sci, 10:1003. https://doi.org/10.3389/fpls.2019.01003
Jiao YQ, Wang YH, Xue DW, et al., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet, 42(6):541–544. https://doi.org/10.1038/ng.591
Jorrín-Novo JV, Maldonado AM, Echevarria-Zomeno S, et al., 2009. Plant proteomics update (2007–2008): secondgeneration proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge. J Proteomics, 72(3):285–314. https://doi.org/10.1016/j.jprot.2009.01.026
Kausch AP, Nelson-Vasilchik K, Hague J, et al., 2019. Edit at will: genotype independent plant transformation in the era of advanced genomics and genome editing. Plant Sci, 281: 186–205. https://doi.org/10.1016/j.plantsci.2019.01.006
Kauss D, Bischof S, Steiner S, et al., 2012. FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway. FEBS Lett, 586(3):211–216. https://doi.org/10.1016/j.febslet.2011.12.029
Kim S, Kim D, Cho SW, et al., 2014. Highly efficient RNAguided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res, 24(6): 1012–1019. https://doi.org/10.1101/gr.171322.113
Kleinstiver BP, Tsai SQ, Prew MS, et al., 2016. Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat Biotechnol, 34(8):869–874. https://doi.org/10.1038/nbt.3620
Leppek K, Das R, Barna M, 2018. Functional 5' UTR mRNA structures in eukaryotic translation regulation and how to find them. Nat Rev Mol Cell, 19(3):158–174. https://doi.org/10.1038/nrm.2017.103
Li AX, Jia SG, Yobi A, et al., 2018. Editing of an alphakafirin gene family increases, digestibility and protein quality in sorghum. Plant Physiol, 177(4):1425–1438. https://doi.org/10.1104/pp.18.00200
Li JF, Norville JE, Aach J, et al., 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol, 31(8):688–691. https://doi.org/10.1038/nbt.2654
Li T, Liu B, Spalding MH, et al., 2012. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 30(5):390–392. https://doi.org/10.1038/nbt.2199
Li T, Liu B, Chen CY, et al., 2016. TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genomic, 43(5):297–305. https://doi.org/10.1016/j.jgg.2016.03.005
Li WT, Zhu ZW, Chern M, et al., 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell, 170(1):114–126. https://doi.org/10.1016/j.cell.2017.06.008
Li YB, Fan CC, Xing YZ, et al., 2011. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet, 43(12):1266–1269. https://doi.org/10.1038/ng.977
Liang XQ, Potter J, Kumar S, et al., 2015. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J Biotechnol, 208:44–53. https://doi.org/10.1016/j.jbiotec.2015.04.024
Lin CS, Hsu CT, Yang LH, et al., 2018. Application of protoplast technology to CRISPR/Cas9 mutagenesis: from singlecell mutation detection to mutant plant regeneration. Plant Biotechnol J, 16(7):1295–1310. https://doi.org/10.1111/pbi.12870
Lin S, Zhao YY, Zhu YF, et al., 2016. An effective and inducible system of TAL effector-mediated transcriptional repression in Arabidopsis. Mol Plant, 9(11):1546–1549. https://doi.org/10.1016/j.molp.2016.09.003
Liu SM, Jiang J, Liu Y, et al., 2019. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Sci, 26(2):88–97. https://doi.org/10.1016/j.rsci.2019.01.002
Lloyd A, Plaisier CL, Carroll D, et al., 2005. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA, 102(6):2232–2237. https://doi.org/10.1073/pnas.0409339102
Mahfouz MM, Li LX, Shamimuzzaman M, et al., 2011. De novoengineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA, 108(6):2623–2628. https://doi.org/10.1073/pnas.1019533108
Mao YF, Botella JR, Liu YG, et al., 2019. Gene editing in plants: progress and challenges. Natl Sci Rev, 6(3):421–437. https://doi.org/10.1093/nsr/nwz005
Meskauskiene R, Nater M, Goslings D, et al., 2001. FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA, 98(22):12826–12831. https://doi.org/10.1073/pnas.221252798
Minkenberg B, Xie KB, Yang YN, 2017. Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes. Plant J, 89(3):636–648. https://doi.org/10.1111/tpj.13399
Molla KA, Yang YN, 2019. CRISPR/Cas-mediated base editing: technical considerations and practical applications. Trends Biotechnol, 37(10):1121–1142. https://doi.org/10.1016/j.tibtech.2019.03.008
Morsy M, Gouthu S, Orchard S, et al., 2008. Charting plant interactomes: possibilities and challenges. Trends Plant Sci, 13(4):183–191. https://doi.org/10.1016/j.tplants.2008.01.006
Nekrasov V, Staskawicz B, Weigel D, et al., 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol, 31(8):691–693. https://doi.org/10.1038/nbt.2655
Nishimasu H, Shi X, Ishiguro S, et al., 2018. Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science, 361(6408):1259–1262. https://doi.org/10.1126/science.aas9129
Oikawa T, Maeda H, Oguchi T, et al., 2015. The birth of a black rice gene and its local spread by introgression. Plant Cell, 27(9):2401–2414. https://doi.org/10.1105/tpc.15.00310
Pandiarajan R, Grover A, 2018. In vivo promoter engineering in plants: are we ready? Plant Sci, 277:132–138. https://doi.org/10.1016/j.plantsci.2018.10.011
Piatek A, Ali Z, Baazim H, et al., 2015. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J, 13(4):578–589. https://doi.org/10.1111/pbi.12284
Pierre-Jerome E, Drapek C, Benfey PN, 2018. Regulation of division and differentiation of plant stem cells. Annu Rev Cell Dev Biol, 34(1):289–310. https://doi.org/10.1146/annurev-cellbio-100617-062459
Qin ZR, Wu JJ, Geng SF, et al., 2017. Regulation of FT splicing by an endogenous cue in temperate grasses. Nat Commun, 8:14320. https://doi.org/10.1038/ncomms14320
Reddy ASN, Marquez Y, Kalyna M, et al., 2013. Complexity of the alternative splicing landscape in plants. Plant Cell, 25(10):3657–3683. https://doi.org/10.1105/tpc.113.117523
Ren B, Liu L, Li SF, et al., 2019. Cas9-NG greatly expands the targeting scope of the genome-editing toolkit by recognizing NG and other atypical PAMs in rice. Mol Plant, 12(7):1015–1026. https://doi.org/10.1016/j.molp.2019.03.010
Richter AS, Hochheuser C, Fufezan C, et al., 2016. Phosphorylation of GENOMES UNCOUPLED 4 alters stimulation of Mg chelatase activity in angiosperms. Plant Physiol, 172(3):1578–1595. https://doi.org/10.1104/pp.16.01036
Rodriguez-Leal D, Lemmon ZH, Man J, et al., 2017. Engineering quantitative trait variation for crop improvement by genome editing. Cell, 171(2):470–480.E8. https://doi.org/10.1016/j.cell.2017.08.030
Shan QW, Wang YP, Li J, et al., 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol, 31(8):686–688. https://doi.org/10.1038/nbt.2650
Shan QW, Wang YP, Li J, et al., 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc, 9(10):2395–2410. https://doi.org/10.1038/nprot.2014.157
Shan QW, Zhang Y, Chen KL, et al., 2015. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J, 13(6):791–800. https://doi.org/10.1111/pbi.12312
Shi JR, Gao HR, Wang HY, et al., 2017. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J, 15(2):207–216. https://doi.org/10.1111/pbi.12603
Shimatani Z, Kashojiya S, Takayama M, et al., 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol, 35(5):441–443. https://doi.org/10.1038/nbt.3833
Soyk S, Müller NA, Park SJ, et al., 2017. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet, 49(1):162–168. https://doi.org/10.1038/ng.3733
Sun YW, Jiao GA, Liu ZP, et al., 2017. Generation of highamylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci, 8:298. https://doi.org/10.3389/fpls.2017.00298
Takahashi K, Yamanaka S, 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126(4):663–676. https://doi.org/10.1016/j.cell.2006.07.024
Takenaka M, Zehrmann A, Verbitskiy D, et al., 2013. RNA editing in plants and its evolution. Annu Rev Genet, 47: 335–352. https://doi.org/10.1146/annurev-genet-111212-133519
Tang L, Mao BG, Li YK, et al., 2017. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cdaccumulating indica rice without compromising yield. Sci Rep, 7:14438. https://doi.org/10.1038/s41598-017-14832-9
Tang X, Lowder LG, Zhang T, et al., 2017. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants, 3(3):17018. https://doi.org/10.1038/nplants.2017.18
von Arnim AG, Jia QD, Vaughn JN, 2014. Regulation of plant translation by upstream open reading frames. Plant Sci, 214:1–12. https://doi.org/10.1016/j.plantsci.2013.09.006
Wang B, Smith SM, Li JY, 2018. Genetic regulation of shoot architecture. Annu Rev Plant Biol, 69(1):437–468. https://doi.org/10.1146/annurev-arplant-042817-040422
Wang FJ, Wang CL, Liu PQ, et al., 2016. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE, 11(4):e0154027. https://doi.org/10.1371/journal.pone.0154027
Wang J, Zhou L, Shi H, et al., 2018. A single transcription factor promotes both yield and immunity in rice. Science, 361(6406):1026–1028. https://doi.org/10.1126/science.aat7675
Wang MG, Mao YF, Lu YM, et al., 2017. Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol Plant, 10(7):1011–1013. https://doi.org/10.1016/j.molp.2017.03.001
Wang SK, Wu K, Yuan QB, et al., 2012. Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet, 44(8): 950–954. https://doi.org/10.1038/ng.2327
Wang SK, Li S, Liu Q, et al., 2015. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet, 47(8):949–954. https://doi.org/10.1038/ng.3352
Wang YP, Cheng X, Shan QW, et al., 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 32(9):947–951. https://doi.org/10.1038/nbt.2969
Woo JW, Kim J, Kwon SI, et al., 2015. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol, 33(11):1162–1164. https://doi.org/10.1038/nbt.3389
Wu L, Zhou HY, Zhang QQ, et al., 2010. DNA methylation mediated by a microRNA pathway. Mol Cell, 38(3):465–475. https://doi.org/10.1016/j.molcel.2010.03.008
Xie KB, Minkenberg B, Yang YN, 2015. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA, 112(11): 3570–3575. https://doi.org/10.1073/pnas.1420294112
Xu CJ, Liu Y, Li YB, et al., 2015. Differential expression of GS5 regulates grain size in rice. J Exp Bot, 66(9):2611–2623. https://doi.org/10.1093/jxb/erv058
Xu RF, Yang YC, Qing RY, et al., 2016. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genomics, 43(8):529–532. https://doi.org/10.1016/j.jgg.2016.07.003
Xue CX, Zhang HW, Lin QP, et al., 2018. Manipulating mRNA splicing by base editing in plants. Sci China Life Sci, 61(11):1293–1300. https://doi.org/10.1007/s11427-018-9392-7
Yang RX, Li PC, Mei HL, et al., 2019. Fine-tuning of miR528 accumulation modulates flowering time in rice. Mol Plant, 12(8):1103–1113. https://doi.org/10.1016/j.molp.2019.04.009
Ytterberg AJ, Jensen ON, 2010. Modification-specific proteomics in plant biology. J Proteomics, 73(11):2249–2266. https://doi.org/10.1016/j.jprot.2010.06.002
Zaidi SSA, Mukhtar MS, Mansoor S, 2018. Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol, 36(9):898–906. https://doi.org/10.1016/j.tibtech.2018.04.005
Zetsche B, Gootenberg JS, Abudayyeh OO, et al., 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPRCas system. Cell, 163(3):759–771. https://doi.org/10.1016/j.cell.2015.09.038
Zhang H, Zhang JS, Lang ZB, et al., 2017. Genome editingprinciples and applications for functional genomics research and crop improvement. Plant Sci, 36(4):291–309. https://doi.org/10.1080/07352689.2017.1402989
Zhang HW, Si XM, Ji X, et al., 2018. Genome editing of upstream open reading frames enables translational control in plants. Nat Biotechnol, 36(9):894–898. https://doi.org/10.1038/nbt.4202
Zhang JS, Zhang H, Botella JR, et al., 2018. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol, 60(5):369–375. https://doi.org/10.1111/jipb.12620
Zhang L, Yu H, Ma B, et al., 2017. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun, 8:14789. https://doi.org/10.1038/ncomms14789
Zhang M, Zhang FL, Fang Y, et al., 2015. The non-canonical tetratricopeptide repeat (TPR) domain of fluorescent (FLU) mediates complex formation with glutamyl-tRNA reductase. J Biol Chem, 290(28):17559–17565. https://doi.org/10.1074/jbc.M115.662981
Zhang YX, Malzahn AA, Sretenovic S, et al., 2019. The emerging and uncultivated potential of CRSIPR technology in plant science. Nat Plants, 5(8):778–794. https://doi.org/10.1038/s41477-019-0461-5
Zhou JP, Deng KJ, Cheng Y, et al., 2017. CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci, 8:1598. https://doi.org/10.3389/fpls.2017.01598
Zhou X, Deng L, Wang Q, et al., 2018. Breeding of waxy rice by genome editing. Mol Plant Breed, 16(17):5608–5615 (in Chinese). https://doi.org/10.13271/j.mpb.016.005608
Zimny T, Sowa S, Tyczewska A, et al., 2019. Certain new plant breeding techniques and their marketability in the context of EU GMO legislation—recent developments. New Biotechnol, 51:49–56. https://doi.org/10.1016/j.nbt.2019.02.003
Zong Y, Song QN, Li C, et al., 2018. Efficient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat Biotechnol, 36(10):950–953. https://doi.org/10.1038/nbt.4261
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We thank Dr. Jen SHEEN (Department of Molecular Biology in Massachusetts General Hospital, Harvard University, USA) for sharing her working progress on the protoplast editing in lettuce, Arabidopsis, and tobacco.
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Yuan-yuan TAN, Hao DU, Xia WU, Yan-hua LIU, Meng JIANG, Shi-yong SONG, Liang WU, and Qing-yao SHU declare that they have no conflict of interest.
This article does not contain any studies with human or animal subjects performed by any of authors.
Project supported by the Zhejiang Provincial S&T Project on Breeding Agricultural (Food) Crops (No. 2016C02050-2) and the National Natural Science Foundation of China (No. 31701394)
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Tan, Yy., Du, H., Wu, X. et al. Gene editing: an instrument for practical application of gene biology to plant breeding. J. Zhejiang Univ. Sci. B 21, 460–473 (2020). https://doi.org/10.1631/jzus.B1900633
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DOI: https://doi.org/10.1631/jzus.B1900633