Current status, challenges, and future prospects of plant genome editing in China

Plant Biotechnology Reports - Tập 13 - Trang 459-472 - 2019
Sulaiman Ahmed1, Yandi Zhang1,2, Muhammad Abdullah3, Qiuxiang Ma1,2, Hongxia Wang1,2, Peng Zhang1,2
1National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Science, Shanghai, China
2University of Chinese Academy of Sciences, Beijing, China
3Agronomy Department, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

Tóm tắt

Genome editing (GE) is the most powerful tool for creating genetic variation in plants. This approach is valuable for studying the mechanism of gene function and regulation as well as to improve desirable traits using sequence-specific endonucleases. It is typically performed with diverse molecular scissors that cleave a particular gene at a defined position. The advent of sequence-specific nucleases such as ZFNs (zinc finger nucleases), TALENs (transcription activator-like effector nucleases), and CRISPR (clustered regularly interspaced short palindromic repeats), in particular, have allowed for the precise and efficient introduction of genetic variation into the genome. The newly developed CRISPR-associated protein 9 (Cas9) variants, base-editing systems, novel RNA-directed nucleases, and DNA-free CRISPR/Cas9 delivery methods offer great opportunities for plant genome engineering. China has made tremendous progress in the field of GE for crop improvement to meet the demand of growing population. Herein, we reviewed the recent progress in GE of different crops in China, highlighting advanced GE tools/methods, and also discussed the specific challenges and prospects of plant GE.

Tài liệu tham khảo

Bai M, Yuan J, Kuang H, Gong P, Li S, Zhang Z, Liu B, Sun J, Yang M, Yang L, Wang D, Song S, Guan Y (2019) Generation of a multiplex mutagenesis population via pooled CRISPR-Cas9 in soybean. Plant Biotechnol J. https://doi.org/10.1111/pbi.13239 Bao AL, Chen HF, Chen LM, Chen SL, Hao QN, Guo W, Qiu DZ, Shan ZH, Yang ZL, Yuan SL, Zhang CJ, Zhang XJ, Liu BH, Kong FJ, Li X, Zhou XA, Tran LSP, Cao D (2019) CRISPR/Cas9-mediated targeted mutagenesis of GmSPL9 genes alters plant architecture in soybean. BMC Plant Biol 19:131 Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712 Basnet R, Zhang JR, Hussain N, Shu QY (2019) Characterization and mutational analysis of a monogalactosyldiacylglycerol synthase gene OsMGD2 in rice. Front Plant Sci 10:992 Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-Type III effectors. Science 326:1509–1512 Cai LL, Cao YY, Xu ZY, Ma WX, Zakria M, Zou LF, Cheng ZQ, Chen GY (2017) A transcription activator-like effector Tal7 of Xanthomonas oryzae pv. oryzicola activates rice gene Os09g29100 to suppress rice immunity. Sci Rep 7:5089 Cai YP, Chen L, Liu XJ, Guo C, Sun S, Wu CX, Jiang BJ, Han TF, Hou WS (2018) CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol J 16:176–185 Cai YP, Chen L, Liu XJ, Sun S, Wu CX, Jiang BJ, Han TF, Hou WS (2015) CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS ONE 10:e0136064 Cai YP, Wang LW, Chen L, Wu TT, Liu LP, Sun S, Wu CX, Yao WW, Jiang BJ, Yuan S, Han TF, Hou WS (2019) Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean. Plant Biotechnol J. https://doi.org/10.1111/pbi.13199 Cao Y, Sun D, Ai H, Mei HY, Liu X, Sun SB, Xu GH, Liu YG, Chen YS, Ma LNQ (2017) Knocking out OsPT4 gene decreases arsenate uptake by rice plants and inorganic arsenic accumulation in rice grains. Environ Sci Technol 51:12131–12138 Curtin SJ, Voytas DF, Stupar RM (2012) Genome engineering of crops with designer nucleases. Plant Genome 5:42–50 Demorest ZL, Coffman A, Baltes NJ, Stoddard TJ, Clasen BM, Luo S, Retterath A, Yabandith A, Gamo ME, Bissen J, Mathis L, Voytas DF, Zhang F (2016) Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biol 16:225 Deyell M, Ameta S, Nghe P (2019) Large scale control and programming of gene expression using CRISPR. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2019.05.013 Du HY, Zeng XR, Zhao M, Cui XP, Wang Q, Yang H, Cheng H, Yu DY (2016) Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol 217:90–97 Duan YB, Li J, Qin RY, Xu RF, Li H, Yang YC, Ma H, Li L, Wei PC, Yang JB (2016) Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol Biol 90:49–62 Fan D, Liu TT, Li CF, Jiao B, Li S, Hou YS, Luo KM (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217 Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232 Fu YF, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826 Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405 Gao CX (2018) The future of CRISPR technologies in agriculture. Nat Rev Mol Cell Biol 19:275–276 Gao JP, Wang GH, Ma SY, Xie XD, Wu XW, Zhang XT, Wu YQ, Zhao P, Xia QY (2015) CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 87:99–110 Gao JP, Zhang T, Xu BX, Jia L, Xiao BG, Liu H, Liu LJ, Yan H, Xia QY (2018a) CRISPR/Cas9-mediated mutagenesis of carotenoid cleavage dioxygenase 8 (CCD8) in tobacco affects shoot and root architecture. Int J Mol Sci 19:E1062 Gao W, Xu WT, Huang KL, Guo MZ, Luo YB (2018b) Risk analysis for genome editing-derived food safety in China. Food Control 84:128–137 Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadan AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71 Geng Y, Zhang P, Liu Q, Wei Z, Riaz A, Chachar S, Gu X (2019) Rice homolog of sin3-associated polypeptide 30, OsSFL1, mediates histone deacetylation to regulate flowering time during short days. Plant Biotechnol J. https://doi.org/10.1111/pbi.13235 Gorbunova V, Levy AA (1999) How plants make ends meet: DNA double-strand break repair. Trends Plant Sci 4:263–269 Gupta D, Bhattacharjee O, Mandal D, Sen MK, Dey D, Dasgupta A, Kazi TA, Gupta R, Sinharoy S, Acharya K, Chattopadhyay D, Ravichandiran V, Roy S, Ghosh D (2019) CRISPR-Cas9 system: A new-fangled dawn in gene editing. Life Sci 232:116636 Hao LI, Ruiying QIN, Xiaoshuang LIU, Shengxiang LIAO, Rongfang XU, Jianbo YANG, Pengcheng WEI (2019) CRISPR/Cas9-mediated adenine base editing in rice genome. Rice Sci 26:125–128 Hiom K (2010) Coping with DNA double strand breaks. DNA Repair 9:1256–1263 Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li YQ, Fine EJ, Wu XB, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31:827–832 Hu BW, Li DW, Liu X, Qi JJ, Gao DL, Zhao SQ, Huang SW, Sun JJ, Yang L (2017) Engineering non-transgenic gynoecious cucumber using an improved transformation protocol and optimized CRISPR/Cas9 system. Mol Plant 10:1575–1578 Hu JC, Li SY, Li ZL, Li HY, Song WB, Zhao HM, Lai JS, Xia LQ, Li DW, Zhang YL (2019) A barley stripe mosaic virus-based guide RNA delivery system for targeted mutagenesis in wheat and maize. Mol Plant Pathol. https://doi.org/10.1111/mpp.12849 Hua K, Tao X, Liang W, Zhang Z, Gou R, Zhu J-K (2019a) Simplified adenine base editors improve adenine base editing efficiency in rice. Plant Biotechnol J. https://doi.org/10.1111/pbi.13244 Hua K, Tao XP, Zhu JK (2019b) Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J 17:499–504 Huang Y, Guo YM, Liu YT, Zhang F, Wang ZK, Wang HY, Wang F, Li DP, Mao DD, Luan S, Liang MZ, Chen LB (2018) 9-cis-Epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Front Plant Sci 9:162 Ji X, Zhang HW, Zhang Y, Wang YP, Gao CX (2015) Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat Plants 1:15144 Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9:e93806 Jiang WY, Marraffini LA (2015) CRISPR-Cas: new tools for genetic manipulations from bacterial immunity systems. Annu Rev Microbiol 69:209–228 Joung JK, Sander JD (2013) INNOVATION TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55 Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93:1156–1160 Kujur A, Saxena MS, Bajaj D, Parida SK (2013) Integrated genomics and molecular breeding approaches for dissecting the complex quantitative traits in crop plants. J Biosci 38:971–987 Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392 Li J, Meng XB, Zong Y, Chen KL, Zhang HW, Liu JX, Li JY, Gao CX (2016a) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2:16139 Li MR, Li XX, Zhou ZJ, Wu PZ, Fang MC, Pan XP, Lin QP, Luo WB, Wu GJ, Li HQ (2016b) Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci 7:377 Li C, Unver T, Zhang BH (2017a) A high-efficiency CRISPR/Cas9 system for targeted mutagenesis in cotton (Gossypium hirsutum L). Sci Rep 7:43902 Li CX, Liu CL, Qi XT, Wu YC, Fei XH, Mao L, Cheng BJ, Li XH, Xie CX (2017b) RNA-guided Cas9 as an invivo desired-target mutator in maize. Plant Biotechnol J 15:1566–1576 Li J, Zhang HW, Si XM, Tian YH, Chen KL, Liu JX, Chen HB, Gao CX (2017c) Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. J Genet Genom 44:465–468 Li JY, Sun YW, Du JL, Zhao YD, Xia LQ (2017d) Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol Plant 10:526–529 Li P, Li YJ, Zhang FJ, Zhang GZ, Jiang XY, Yu HM, Hou BK (2017e) The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J 89:85–103 Li C, Zong Y, Wang YP, Jin S, Zhang DB, Song QN, Zhang R, Gao CX (2018a) Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19:59 Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018b) Multiplexed CRISPR/Cas9-mediated metabolic engineering of gamma-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16:415–427 Li XS, Wang Y, Liu YJ, Yang B, Wang X, Wei J, Lu ZY, Zhang YX, Wu J, Huang XX, Yang L, Chen J (2018c) Base editing with a Cpf1-cytidine deaminase fusion. Nat Biotechnol 36:324–327 Li CY, Li W, Zhou ZH, Chen H, Xie CH, Lin YJ (2019a) A new rice breeding method: CRISPR/Cas9 system editing of the Xa13 promoter to cultivate transgene-free bacterial blight-resistant rice. Plant Biotechnol J. 25:1–3 Li H, Qin RY, Liu XS, Liao SX, Xu RF, Yang JB, Wei PC (2019b) CRISPR/Cas9-mediated adenine base editing in rice genome. Rice Sci 26:125–128 Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41:63–68 Liu S, Jiang J, Liu Y, Meng J, Xu S, Tan Y, Li Y, Shu Q, Huang J (2019) Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Sci 26:88–97 Lou DJ, Wang HP, Liang G, Yu DQ (2017) OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci 8:993 Lu YM, Zhu JK (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mo Plant 10:523–525 Ma XL, Mau M, Sharbel TF (2018) Genome editing for global food security. Trends Biotechnol 36:123–127 Mao YF, Botella JR, Liu YG, Zhu JK (2019) Gene editing in plants: progress and challenges. Natl Sci Rev 6:421–437 Mao YF, Zhang H, Xu NF, Zhang BT, Gou F, Zhu JK (2013) Application of the CRISPR–Cas system for efficient genome engineering in plants. Mol Plant 6:2008–2011 Marraffini LA (2015) CRISPR-Cas immunity in prokaryotes. Nature 526:55–61 Miao CB, Wang D, He RQ, Liu SK, Zhu JK (2019) Mutations in MIR396e and MIR396f increase grain size and modulate shoot architecture in rice. Plant Biotechnol J. https://doi.org/10.1111/pbi.13214 Miao J, Guo DS, Zhang JZ, Huang QP, Qin GJ, Zhang X, Wan JM, Gu HY, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23:1233–1236 Miller JC, Holmes MC, Wang JB, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO, Rebar EJ (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25:778–785 Miller JC, Zhang L, Xia DF, Campo JJ, Ankoudinova IV, Guschin DY, Babiarz JE, Meng XD, Hinkley SJ, Lam SC, Paschon DE, Vincent AI, Dulay GP, Barlow KA, Shivak DA, Leung E, Kim JD, Amora R, Urnov FD, Gregory PD, Rebarsimplicity EJ (2015) Improved specificity of TALE-based genome editing using an expanded RVD repertoire. Nat Methods 12:465–471 Pan CT, Ye L, Qin L, Liu X, He YJ, Wang J, Chen LF, Lu G (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:24765 Peng AH, Chen SC, Lei TG, Xu LZ, He YR, Wu L, Yao LX, Zou XP (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15:1509–1519 Petolino JF (2015) Genome editing in plants via designed zinc finger nucleases. Vitro Cell Dev Biol Plant 51:1–8 Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14 Qin L, Li J, Wang Q, Xu Z, Sun L, Alariqi M, Manghwar H, Wang G, Li B, Ding X, Rui H, Huang H, Lu T, Lindsey K, Daniell H, Zhang X, Jin S (2019) High-efficient and precise base editing of CG to TA in the allotetraploid cotton (Gossypium hirsutum) genome using a modified CRISPR/Cas9 system. Plant Biotechnol J. https://doi.org/10.1111/pbi.13168 Ren B, Liu L, Li SF, Kuang YJ, Wang JW, Zhang DW, Zhou XP, Lin HH, Zhou HB (2019) Cas9-NG greatly expands the targeting scope of the genome-editing toolkit by recognizing NG and other atypical PAMs in rice. Mol Plant 12:1015–1026 Ren B, Yan F, Kuang YJ, Li N, Zhang DW, Zhou XP, Lin HH, Zhou HB (2018) Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant. Mol Plant 11:623–626 Ren C, Liu XJ, Zhang Z, Wang Y, Duan W, Li SH, Liang ZC (2016) CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L). Sci Rep 6:32289 Ricroch A, Harwood W, Svobodova Z, Sagi L, Hundleby P, Badea EM, Rosca I, Cruz G, Salema Fevereiro MP, Marfa Riera V, Jansson S, Morandini P, Bojinov B, Cetiner S, Custers R, Schrader U, Jacobsen HJ, Martin-Laffon J, Boisron A, Kuntz M (2016) Challenges facing European agriculture and possible biotechnological solutions. Crit Rev Biotechnol 36:875–883 Shan QW, Wang YP, Li J, Zhang Y, Chen KL, Liang Z, Zhang K, Liu JX, Xi JJ, Qiu JL, Gao CX (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688 Shan QW, Zhang Y, Chen KL, Zhang K, Gao CX (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800 Shen CX, Que ZQ, Xia YM, Tang N, Li D, He RH, Cao ML (2017) Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol 60:539–547 Shen L, Wang C, Fu YP, Wang JJ, Liu Q, Zhang XM, Yan CJ, Qian Q, Wang KJ (2018) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol 60:89–93 Shi JR, Gao HR, Wang HY, Lafitte HR, Archibald RL, Yang MZ, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216 Sun YW, Jiao GA, Liu ZP, Zhang X, Li JY, Guo XP, Du WM, Du JL, Francis F, Zhao YD, Xia LQ (2017) Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci 8:298 Sun YW, Zhang X, Wu CY, He YB, Ma YZ, Hou H, Guo XP, Du WM, Zhao YD, Xia LQ (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9:628–631 Sun ZJ, Li NZ, Huang GD, Xu JQ, Pan Y, Wang ZM, Tang QL, Song M, Wang XJ (2013) Site-specific gene targeting using transcription activator-like effector (TALE)-based nuclease in Brassica oleracea. J Integr Plant Biol 55:1092–1103 Tang J, Wang Y-Q, Yin W, Dong G, Sun K, Teng Z, Wu X, Wang S, Qian Y, Pan X, Qian Q, Chu C (2019) Mutation of a nucleotide-binding leucine-rich repeat immune receptor-type protein disrupts immunity to bacterial blight. Plant Physiol. https://doi.org/10.1104/pp.19.00686 Tang L, Mao BG, Li YK, Lv QM, Zhang LP, Chen CY, He HJ, Wang WP, Zeng XF, Shao Y, Pan YL, Hu YY, Peng Y, Fu XQ, Li HQ, Xia ST, Zhao BR (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:14438 Tang T, Yu X, Yang H, Gao Q, Ji H, Wang Y, Yan G, Peng Y, Luo H, Liu K, Li X, Ma C, Kang C, Dai C (2018) Development and validation of an effective CRISPR/Cas9 vector for efficiently Isolating positive transformants and transgene-free mutants in a wide range of plant species. Front Plant Sci 9:1533 Tian SW, Jiang LJ, Cui XX, Zhang J, Guo SG, Li MY, Zhang HY, Ren Y, Gong GY, Zong M, Liu F, Chen QJ, Xu Y (2018) Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep 37:1353–1356 Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX, Gao CX, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951 Wang FJ, Wang CL, Liu PQ, Lei CL, Hao W, Gao Y, Liu YG, Zhao KJ (2016a) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 11:e0154027 Wang LX, Wang LL, Tan Q, Fang QL, Zhu H, Hong ZL, Zhang ZM, Duanmu DQ (2016b) Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus using CRISPR-Cas9. Front Plant Sci 7:1333 Wang FJ, Wang CL, Zheng CK, Qin TF, Gao Y, Liu PQ, Zhao KJ (2017a) Creation of gene-specific rice mutants by AvrXa23-based TALENs. J Integr Agric 16:424–434 Wang FZ, Chen MX, Yu LJ, Xie LJ, Yuan LB, Qi H, Xiao M, Guo WX, Chen Z, Yi KK, Zhang JH, Qiu RL, Shu WS, Xiao S, Chen QF (2017b) OsARM1, an R2R3 MYB transcription factor, is involved in regulation of the response to arsenic stress in rice. Front Plant Sci 8:1868 Wang L, Chen L, Li R, Zhao RR, Yang MJ, Sheng JP, Shen L (2017c) Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J Agric Food Chem 65:8674–8682 Wang W, Pan Q, He F, Akhunova A, Chao S, Trick H, Akhunov E (2018a) Transgenerational CRISPR-Cas9 activity facilitates multiplex gene editing in allopolyploid wheat. CRISPR J 1:65–74 Wang XH, Tu MX, Wang DJ, Liu JW, Li YJ, Li Z, Wang YJ, Wang XP (2018b) CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnol J 16:844–855 Wang BB, Zhu L, Zhao BB, Zhao YP, Xie YR, Zheng ZG, Li YY, Sun J, Wang HY (2019a) Development of a haploid-Inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12:597–602 Wang C, Liu Q, Shen Y, Hua YF, Wang JJ, Lin JR, Wu MG, Sun TT, Cheng ZK, Mercier R, Wang KJ (2019b) Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol 37:283–286 Wang J, Liu X, Zhang A, Ren Y, Wu F, Wang G, Xu Y, Lei C, Zhu S, Pan T, Wang Y, Zhang H, Wang F, Tan Y-Q, Wang Y, Jin X, Luo S, Zhou C, Zhang X, Liu J, Wang S, Meng L, Wang Y, Chen X, Lin Q, Zhang X, Guo X, Cheng Z, Wang J, Tian Y, Liu S, Jiang L, Wu C, Wang E, Zhou J-M, Wang Y-F, Wang H, Wan J (2019c) A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice. Cell Res. 29:820–831 Wang L, Rubio MC, Xin X, Zhang B, Fan Q, Wang Q, Ning G, Becana M, Duanmu D (2019d) CRISPR/Cas9 knockout of leghemoglobin genes in Lotus japonicus uncovers their synergistic roles in symbiotic nitrogen fixation. New Phytol. https://doi.org/10.1111/nph.16077 Wang HX, Wu YL, Zhang YD, Yang J, Fan WJ, Zhang H, Zhao SS, Yuan L, Zhang P (2019e) CRISPR/Cas9-based mutagenesis of starch biosynthetic genes in sweet potato (Ipomoea Batatas) for the improvement of starch quality. Int J Mol Sci 20:4702 Weeks DP, Spalding MH, Yang B (2016) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J 14:483–495 Wu WY, Lebbink JH, Kanaar R, Geijsen N, Van Der Oost J (2018) Genome editing by natural and engineered CRISPR-associated nucleases. Nat Chem Biol 14:642–651 Xie E, Li Y, Tang D, Lv Y, Shen Y, Cheng Z (2019) A strategy for generating rice apomixis by gene editing. J Integr Plant Biol 61:911–916 Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, Wei P, Yang J (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genom 43:529–532 Xu RF, Li H, Qin RY, Wang L, Li L, Wei PC, Yang JB (2014) Gene targeting using the Agrobacteriumtumefaciens-mediated CRISPR-Cas system in rice. Rice 7:5 Yamamoto T, Kashojiya S, Kamimura S, Kameyama T, Ariizumi T, Ezura H, Miura K (2018) Application and development of genome editing technologies to the solanaceae plants. Plant Physiol Biochem 131:37–46 Yan F, Kuang YJ, Ren B, Wang JW, Zhang DW, Lin HH, Yang B, Zhou XP, Zhou HB (2018) Highly efficient A.T to G.C base editing by Cas9n-guided tRNA adenosine deaminase in rice. Mol Plant 11:631–634 Yang Y, Zhu K, Li H, Han S, Meng Q, Khan SU, Fan C, Xie K, Zhou Y (2018) Precise editing of CLAVATA genes in Brassica napus L. regulates multilocular silique development. Plant Biotechnol J 16:1322–1335 Yao L, Zhang Y, Liu CX, Liu YB, Wang YL, Liang DW, Liu JT, Sahoo G, Kelliher T (2018) OsMATL mutation induces haploid seed formation in indica rice. Nat Plants 4:530–533 Ye Y, Li P, Xu TQ, Zeng LT, Cheng D, Yang M, Luo J, Lian XM (2017a) OsPT4 contributes to arsenate uptake and transport in rice. Front Plant Sci 8:2197 Ye J, Wang X, Hu TX, Zhang FX, Wang B, Li CX, Yang TX, Li HX, Lu YG, Giovannoni JJ, Zhang YY, Ye ZB (2017b) An InDel in the promoter of Al-activated malate transporter9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell 29:2249–2268 Yu QH, Wang BK, Li N, Tang YP, Yang SB, Yang T, Xu J, Guo CM, Yan P, Wang Q, Asmutola P (2017) CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf life tomato lines. Sci Rep 7:11874 Zhang H, Zhang JS, Wei PL, Zhang BT, Gou F, Feng ZY, Mao YF, Yang L, Zhang H, Xu NF, Zhu JK (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807 Zhang JS, Zhang H, Botella JR, Zhu JK (2018) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol 60:369–375 Zhang R, Liu JX, Chai ZZ, Chen S, Bai Y, Zong Y, Chen KL, Li JY, Jiang LJ, Gao CX (2019) Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing. Nat Plants 5:480–485 Zhang Y, Liang Z, Zong Y, Wang YP, Liu JX, Chen KL, Qiu JL, Gao CX (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617 Zhang YW, Bai Y, Wu GH, Zou SH, Chen YF, Gao CX, Tang DZ (2017) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J 91:714–724 Zheng M, Zhang L, Tang M, Liu JL, Liu HF, Yang HL, Fan SH, Terzaghi W, Wang HZ, Hua W (2019) Knockout of two BnaMAX1 homologs by CRISPR/Cas9-targeted mutagenesis improves plant architecture and increases yield in rapeseed (Brassica napus L.). Plant Biotechnol J. https://doi.org/10.1111/pbi.13228 Zhou JH, Peng Z, Long JY, Sosso D, Liu B, Eom JS, Huang S, Liu SZ, Cruz CV, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643 Zong Y, Song QN, Li C, Jin S, Zhang DB, Wang YP, Qiu JL, Gao CX (2018) Efficient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat Biotechnol 36:950–953 Zong Y, Wang YP, Li C, Zhang R, Chen KL, Ran YD, Qiu JL, Wang DW, Gao CX (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440