Abstract
Improving crops through plant breeding, an important approach for sustainable agriculture, has been utilized to increase the yield and quality of foods and other biomaterials for human use. Crops, including cereals, vegetables, ornamental flowers, fruits, and trees, have long been cultivated to produce high-quality products for human consumption. Conventional breeding technologies, such as natural cross-hybridization, mutation induction through physical or chemical mutagenesis, and modern transgenic tools are often used to enhance crop production. However, these breeding methods are sometimes laborious and complicated, especially when attempting to improve desired traits without inducing pleiotropic effects. Recently, targeted genome editing (TGE) technology using engineered nucleases, including meganucleases, zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced short palindromic repeat (CRISPR) nucleases, has been used to improve the traits of economically important plants. TGE has emerged as a novel plant-breeding tool that represents an alternative approach to classical breeding, but with higher mutagenic efficiency. Here, we briefly describe the basic principles of TGE and the types of engineered nucleases utilized, along with their advantages and disadvantages. We also discuss their potential use to improve the traits of horticultural crops through genome engineering.
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Literature Cited
Abiri R, Valdiani A, Maziah M, Shaharuddin NA, Sahebi M, Yusof Zy, Atabaki N, Talei D (2015) A critical review of the concept of transgenic plants: insights into pharmaceutical biotechnology and molecular farming. Curr Issues Mol Biol 18:21–42
Ainley WM, Sastry-Dent L, Welter ME, Murray MG, Zeitler B, Amora R, Corbin DR, Miles RR, Arnold NL, et al (2013) Trait stacking via targeted genome editing. Plant Biotechnol J 11:1126–1134
Albert NW, Davies KM, Lewis DH, Zhang H, Montefiori M, Brendolise C, Boase MR, Ngo Hanh, Jameson PE, et al (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26:962–980
Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM (2015) CRISPR/Cas9-mediated viral interference in plants. Genome Biol 16:238
Allard RW (1999) Principles of plant breeding. John Wiley & Sons, New York, USA.
Araki M, Ishii T (2015) Towards social acceptance of plant breeding by genome editing. Trends Plant Sci 20:145–149
Araki M, Ishii T (2016) Consumer acceptance of food crops developed by genome editing. Plant Cell Rep 35:1507–1518
Arnould S, Perez C, Cabaniols JP, Smith J, Gouble A, Grizot S, Epinat JC, Duclert A, Duchateau P, et al. (2007) Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells. J Mol Biol 371:49–65
Beetham PR, Kipp PB, Sawycky XL, Arntzen CJ, May GD (1999) A tool for functional plant genomics: Chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations. Proc Nat Acad Sci USA 96:8774–8778
Bibikova M, Golic M, Golic KG, Carroll D (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161:1169–1175
Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bona U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512
Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated 9 system. Plant Physiol 166:1292–1297
Brunet E, Simsek D, Tomishima M, DeKelver R, Choi VM, Gregory P et al. (2009) Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci USA 106:10620–10625
Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, Diergaarde P, Groenendijk J, et al (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
Carroll D (2014) Genome engineering with targetable nucleases. Annu Rev Biochem 83:409–439
Center_for_Food_Safety (2015) Environmental, Farmer, and Consumer Groups Demand Higher Standards for Genetically Engineered (GE) Crop Regulations. http://www.centerforfoodsafety.org/press-releases/3967/environmental-farmer-and-consumergroups-demand-higher-s tandards-for-genetically-engineered-gecrop-regulations. Accessed 19 Feb 2016
Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, et al (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39, e82.
Char SN, Unger-Wallace E, Frame B, Briggs SA, Main M, Spalding MH, Vollbrecht E, Wang K, Yang B (2015) Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J 13:1002–1010
Chen W, Qian Y, Wu X, Sun Y, Wu X, Cheng X (2014) Inhibiting replication of begomoviruses using artificial zinc finger nucleases that target viral-conserved nucleotide motif. Virus Genes 48:494–501
Chevalier BS, Kortemme T, Chadsey MS, Baker D, Monnat RJ, Stoddard BL (2002) Design, activity, and structure of a highly specific artificial endonuclease. Mol Cell 10:895–905
Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24:132–141
Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A et al. (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761
Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, et al. (2015) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176
D’Halluin K, Vanderstraeten C, Van Hulle J, Rosolowska J, Van Den Brande I, Pennewaert A, D’Hont K, Bossut M, Jantz D, et al (2013) Targeted molecular trait stacking in cotton through targeted double-strand break induction. Plant Biotechnol J 11:933–941
Davis AJ, Chen DJ (2013) DNA double strand break repair via non-homologous end-joining. Transl Cancer Res 2:130–143
DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41:4336–4343
Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, et al (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76:888–899
Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096
Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, et al (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26:702–708
Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S (2005) Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 18:5978–5990
Endo M, Mikami, M, Toki S (2016) Biallelic gene targeting in rice. Plant Physiol 170:667–677
Epinat JC, Arnould S, Chames P, Rochaix P, Desfontaines D, Puzin C, Patin A, Zanghellini A, Paques F, et al. (2003) A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res 31:2952–2962
Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015). Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217
Forkmann G, Martens S (2001) Metabolic engineering and applications of flavonoids. Curr Opin Biotechnol 12:155–160
Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK et al (2013) High-frequency offtarget mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826
Gaj T, Gersbach CA, Barbas CF III (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, et al (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187
Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q (2015a) CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 87:99–110
Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y (2015b) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci USA 112:2275–2280
GM_Freeze (2016) The case for regulating gene edited crops. http://www.gmfreeze.org/news-releases/266/. Accessed 7 Mar 2016
Gregory PJ, Johnson SN, Newton AC, Ingram JS (2009) Integrating pests and pathogens into the climate change/food security debate. J Exp Bot 60:2827–2838
Gupta M, DeKelver RC, Palta A, Clifford C, Gopalan S, Miller JC, Novak S, Desloover D, Gachotte D, et al (2012) Transcriptional activation of Brassica napus beta-ketoacyl-ACP synthase II with an engineered zinc finger protein transcription factor. Plant Biotechnol J 10:783–791
Gürlevik E, Schache P, Goez A, Kloos A, Woller N, Armbrecht N, Manns MP, Kubicka S, Kühnel F (2013) Meganuclease-mediated virus self-cleavage facilitates tumor-specific virus replication. Mol Ther 21:1738–1748
Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, et al (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12:934–940
Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiao Y, et al (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29:731–734
Hou Z, Zhang Y, Propson NE, Howden SE, Chu L-F, Sontheimer EJ, Thomson JA (2013) Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci USA 110:15644–15649
Hyun Y, Kim J, Cho SW, Choi Y, Kim JS, Coupland G (2015) Sitedirected mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta 241:271–284
Jaggard KW, Qi AM, Ober ES (2010) Possible changes to arable crop yields by 2050. Phil Trans R Soc B: Biol Sci 365:2835–2851
Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nature Plants 1:15144
Jiang CJ, Shimono M, Maeda S, Inoue H, Mori M, Hasegawa M, Sugano S, Takatsuji H (2009) Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol Plant-Microbe Interact 22:820–829
Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41:e188
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821
Joung JK, Sander JD (2013) TALENs: awidely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55
Kanchiswamy CN, Malnoy M, Velasco R, Kim JS, Viola R (2015) Non-GMO genetically edited crop plants. Trends Biotechnol 33:489–491
Kim S, Kim D, Cho SW, Kim J, Kim JS (2014) Highly efficient RNA guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res 24:1012–1019
Kraft K, Geuer S, Will AJ, Chan WL, Paliou C, Borschiwer M, Harabula I, Wittler L, Franke M, et al (2015) Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep 10:833–839
Lawrenson T, Shorinola O, Stacey N, Li C, Ostergaard L, Patron N, Uauy C, Harwood W (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16:258
Lee, HJ, Kweon J, Kim E, Kim S, Kim JS (2012) Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 22:539–548
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 X, Heyer WD (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Res 18:99–113
Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant 54:569–581
Liu Y, Yang H, Sakanishi A (2006) Ultrasound: mechanical gene transfer into plant cells by sonoporation. Biotechnol Adv 24:1–16
Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci USA 102:2232–2237
Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, et al. (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319:607–610
Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE (2014) Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol 166:1288–1291
Luo S, Li J, Stoddard TJ, Baltes NJ, Demorest ZL, Clasen BM, Coffman A, Retterath A, Mathis L, Voytas DF, et al (2015) Non-transgenic plant genome editing using purified sequence-specific nucleases. Mol Plant 8:1425–1427
Ma S, Wang X, Liu Y, Gao J, Zhang S, Shi R, Chang J, Zhao P, Xia Q (2014) Multiplex genomic structure variation mediated by TALEN and ssODN. BMC Genomics 15:41
Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, et al (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467–477
Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE et al (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
Martin-Ortigosa S, Valenstein JS, Lin VS, Trewyn BG, Wang K (2012) Gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method. Adv Funct Mater 22:3576–3582
Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, et al (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotech 25:778–785
Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehar Y, Tanji M, Sato M, Nasu S, et al. (2002) Positional cloning of rice semi dwarfing gene, sd-1: “rice green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9:11–17
Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147:969–977
Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T (2011). A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39:9283–9293
Napier JA, Haslam RP, Beaudoin F, Cahoon EB (2014) Understanding and manipulating plant lipid composition: Metabolic engineering leads the way. Curr Opin Plant Biol 19:68–75
Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289
Ottaviani D, LeCain M, Sheer D (2014) The role of microhomology in genomic structural variation. Trends Genet 30:85–94
Pacher M, Schmidt-Puchta W, Puchta H (2007) Two unlinked doublestrand breaks can induce reciprocal exchanges in plant genomes via homologous recombination and nonhomologous end joining. Genetics 175:21–29
Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, Liu O et al (2008) Establishment of HIV-1 resistance in CD41 T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26:808–816
Roth N, Klimesch J, Dukowic-Schulze S, Pacher M, Mannuss A, Puchta H (2012) The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells. Plant J 72:781–790
Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JRJ (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29:697–698
Sawai S, Ohyama K, Yasumoto S, Seki H, Sakuma T, Yamamoto T, Kakebayashi Y, Kojima M, Sakakibara H, et al (2014) Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato. Plant Cell 26:3763–3774
Schlenker W, Roberts MJ (2009) Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change. Proc Natl Acad Sci USA 106:15594–15598
Schomburg FM, Bizzell, CM, Lee DL, Zeevaart, JAD, Amasino RM (2003) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15:151-163
Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800
Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987
Shibuya K, Barry KG, Ciardi JA, Loucas HM, Underwood BA, Nourizadeh S, Ecker JR, Klee HJ, Clark DG (2004) The central role of PhEIN2 in ethylene responses throughout plant development in petunia. Plant Physiol 136:2900–2912
Shu QY (2009) Turning plant mutation breeding into a new era: molecular mutation breeding. Induced plant mutations in the genomics era. Rome: FAO:425–427
Shukla VK, Doyon, Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, et al. (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441
Sikora P, Chawade A, Larsson M, Olsson J, Olsson O (2011) Mutagenesis as a tool in plant genetics, functional genomics, and breeding. Int J Plant Genomics 314:829
Stoddard BL (2011) Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modification. Structure 19:7–15
Subburaj S, Cao S, Xia X, He Z (2016a) Phylogenetic analysis, lineage-specific expansion and functional divergence of seed dormancy 4-like genes in plants. PLoS ONE 11:e0153717
Subburaj S, Chung SJ, Lee C, Ryu SM, Kim DH, Kim JS, Bae S, Lee GJ (2016b) Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep 35:1535–1544
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, et al. (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci USA 107:5792–5797
The Council of the European Communities (1990) Council Directive 90/220/ EEC of 23 April 1990 on the deliberate release into the environment of genetically modified organisms. Office J 117:15–27
Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445
Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, Jamieson AC, Porteus MH, Gregory PD, et al (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646–651
van Nocker S, Gardiner SE (2014) Breeding better cultivars, faster: applications of new technologies for the rapid deployment of superior horticultural tree crops. Hortic Res 1:14022
Walt Z (2016) Gene-edited CRISPR mushroom escapes US regulation. Nature News 532:293
Wang F, Wang C, Liu P, Lei C, Hao W, Gao Y, Liu YG, Zhao K (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 11:e0154027
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C et al (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951
Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch-Pedersen H, Holme IB (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83:279–285
White FF, Yang B (2009) Host and pathogen factors controlling the rice-Xanthomonas oryzae interaction Plant Physiol 150:1677–1686
Wolt JD, Wang K, Yang B (2016) The regulatory status of genome-edited crops. Plant Biotechnol J 14:510–518
Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, et al (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnol 33:1162–1164
Wyman C, Kanaar R (2006) DNA double-strand break repair: all’s well that ends well. Annu Rev Genet 40:363–383
Xiong JS, Ding J, Li Y (2016) Genome-editing technologies and their potential application in horticultural crop breeding. Hort Res 2:15019
Xu Y (2010) Molecular Plant Breeding. CABI.
Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, Deng W, Li Z (2010) Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. J Exp Bot 61:697–708
Younis A, Siddique MI, Kim CK, Lim KB (2014) RNA Interference (RNAi) Induced gene silencing: A promising approach of hi-tech plant breeding. Int J Biol Sci 10:1150–1158
Zhou X, Jacobs TB, Xue LJ, Harding SC, Tsai CJ (2015) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. New Phytol 208:298–301
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Subburaj, S., Tu, L., Jin, YT. et al. Targeted genome editing, an alternative tool for trait improvement in horticultural crops. Hortic. Environ. Biotechnol. 57, 531–543 (2016). https://doi.org/10.1007/s13580-016-0281-8
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DOI: https://doi.org/10.1007/s13580-016-0281-8