Targeted Genome Editing, an Alternative Tool for Trait Improvement in Horticultural Crops

다국어 초록 (Multilingual 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.

참고문헌 (Reference)

1 Beetham PR, "tool for functional plant genomics: Chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations" 96 : 8774-8778, 1999

2 Durai S, "Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells" 18 : 5978-5990, 2005

3 Gaj T, "ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering" 31 : 397-405, 2013

4 Napier JA, "Understanding and manipulating plant lipid composition: Metabolic engineering leads the way" 19 : 68-75, 2014

5 Liu Y, "Ultrasound: mechanical gene transfer into plant cells by sonoporation" 24 : 1-16, 2006

6 Pacher M, "Two unlinked doublestrand breaks can induce reciprocal exchanges in plant genomes via homologous recombination and nonhomologous end joining" 175 : 21-29, 2007

7 Shu QY, "Turning plant mutation breeding into a new era:molecular mutation breeding. Induced plant mutations in the genomics era"

8 Gupta M, "Transcriptional activation of Brassica napus beta-ketoacyl-ACP synthase II with an engineered zinc finger protein transcription factor" 10 : 783-791, 2012

9 Ainley WM, "Trait stacking via targeted genome editing" 11 : 1126-1134, 2013

10 Araki M, "Towards social acceptance of plant breeding by genome editing" 20 : 145-149, 2015

11 Ottaviani D, "The role of microhomology in genomic structural variation" 30 : 85-94, 2014

12 Roth N, "The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells" 72 : 781-790, 2012

13 Wolt JD, "The regulatory status of genome-edited crops" 14 : 510-518, 2016

14 Shibuya K, "The central role of PhEIN2 in ethylene responses throughout plant development in petunia" 136 : 2900-2912, 2004

15 GM_Freeze, "The case for regulating gene edited crops"

16 Buschges R, "The barley Mlo gene: a novel control element of plant pathogen resistance" 88 : 695-705, 1997

17 Christian M, "Targeting DNA double-strand breaks with TAL effector nucleases" 186 : 757-761, 2010

18 Lloyd A, "Targeted mutagenesis using zinc-finger nucleases in Arabidopsis" 102 : 2232-2237, 2005

19 Lor VS, "Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases" 166 : 1288-1291, 2014

20 D’Halluin K, "Targeted molecular trait stacking in cotton through targeted double-strand break induction" 11 : 933-941, 2013

21 Sander JD, "Targeted gene disruption in somatic zebrafish cells using engineered TALENs" 29 : 697-698, 2011

22 Lee, HJ, "Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases" 22 : 539-548, 2012

23 Bibikova M, "Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases" 161 : 1169-1175, 2002

24 Joung JK, "TALENs: awidely applicable technology for targeted genome editing" 14 : 49-55, 2013

25 Wendt T, "TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants" 83 : 279-285, 2013

26 Jiang CJ, "Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice" 22 : 820-829, 2009

27 Sawai S, "Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato" 26 : 3763-3774, 2014

28 Hyun Y, "Sitedirected mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles" 241 : 271-284, 2015

29 Subburaj S, "Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9ribonucleoproteins" 35 : 1535-1544, 2016

30 Wang Y, "Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew" 32 : 947-951, 2014

31 Yang Y, "Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato" 61 : 697-708, 2010

32 Mali P, "RNA-guided human genome engineering via Cas9" 339 : 823-826, 2013

33 Younis A, "RNA Interference (RNAi) Induced gene silencing: A promising approach of hi-tech plant breeding" 10 : 1150-1158, 2014

34 Lobell DB, "Prioritizing climate change adaptation needs for food security in 2030" 319 : 607-610, 2008

35 Allard RW, "Principles of plant breeding" John Wiley & Sons 1999

36 Shukla VK, "Precise genome modification in the crop species Zea mays using zinc-finger nucleases" 459 : 437-441, 2009

37 Jaggard KW, "Possible changes to arable crop yields by 2050" 365 : 2835-2851, 2010

38 Monna L, "Positional cloning of rice semi dwarfing gene, sd-1: “rice green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis" 9 : 11-17, 2002

39 Subburaj S, "Phylogenetic analysis, lineage-specific expansion and functional divergence of seed dormancy 4-like genes in plants" 11 : e0153717-, 2016

40 Schomburg FM, "Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants" 15 : 151-163, 2003

41 Schlenker W, "Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change" 106 : 15594-15598, 2009

42 Luo S, "Non-transgenic plant genome editing using purified sequence-specific nucleases" 8 : 1425-1427, 2015

43 Kanchiswamy CN, "Non-GMO genetically edited crop plants" 33 : 489-491, 2015

44 Sikora P, "Mutagenesis as a tool in plant genetics, functional genomics, and breeding" 314829 : 2011

45 Ma S, "Multiplex genomic structure variation mediated by TALEN and ssODN" 15 : 41-, 2014

46 Moose SP, "Molecular plant breeding as the foundation for 21st century crop improvement" 147 : 969-977, 2008

47 Sugimoto K, "Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice" 107 : 5792-5797, 2010

48 Xu Y, "Molecular Plant Breeding"

49 Forkmann G, "Metabolic engineering and applications of flavonoids" 12 : 155-160, 2001

50 Gürlevik E, "Meganuclease-mediated virus self-cleavage facilitates tumor-specific virus replication" 21 : 1738-1748, 2013

51 Djukanovic V, "Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26)using a re-designed I-CreI homing endonuclease" 76 : 888-899, 2013

52 Napoli C, "Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans" 2 : 279-289, 1990

53 Gregory PJ, "Integrating pests and pathogens into the climate change/food security debate" 60 : 2827-2838, 2009

54 Chen W, "Inhibiting replication of begomoviruses using artificial zinc finger nucleases that target viral-conserved nucleotide motif" 48 : 494-501, 2014

55 Lawrenson T, "Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9nuclease" 16 : 258-, 2015

56 Clasen BM, "Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169-176" 14 : 169-176, 2015

57 Li X, "Improvement of biomass through lignin modification" 54 : 569-581, 2008

58 Haun W, "Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family" 12 : 934-940, 2014

59 White FF, "Host and pathogen factors controlling the rice Xanthomonas oryzae interaction" 150 : 1677-1686, 2009

60 Li X, "Homologous recombination in DNA repair and DNA damage tolerance" 18 : 99-113, 2008

61 Stoddard BL, "Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modification" 19 : 7-15, 2011

62 Urnov FD, "Highly efficient endogenous human gene correction using designed zinc-finger nucleases" 435 : 646-651, 2005

63 Kim S, "Highly efficient RNA guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins" 24 : 1012-1019, 2014

64 Fu Y, "High-frequency offtarget mutagenesis induced by CRISPR-Cas nucleases in human cells" 31 : 822-826, 2013

65 Townsend JA, "High-frequency modification of plant genes using engineered zinc-finger nucleases" 459 : 442-445, 2009

66 Li T, "High-efficiency TALEN-based gene editing produces disease-resistant rice" 30 : 390-392, 2012

67 Gao H, "Heritable targeted mutagenesis in maize using a designed endonuclease" 61 : 176-187, 2010

68 Doyon Y, "Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases" 26 : 702-708, 2008

69 Char SN, "Heritable site-specific mutagenesis using TALENs in maize" 13 : 1002-1010, 2015

70 Martin-Ortigosa S, "Gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method" 22 : 3576-3582, 2012

71 Xiong JS, "Genome-editing technologies and their potential application in horticultural crop breeding" 2 : 15019-, 2016

72 Carroll D, "Genome engineering with targetable nucleases" 83 : 409-439, 2014

73 DiCarlo JE, "Genome engineering in Saccharomyces cerevisiae using CRISPR Cas systems" 41 : 4336-4343, 2013

74 Doudna JA, "Genome editing. The new frontier of genome engineering with CRISPR-Cas9" 346 : 1258096-, 2014

75 Hockemeyer D, "Genetic engineering of human pluripotent cells using TALE nucleases" 29 : 731-734, 2011

76 Walt Z, "Gene-edited CRISPR mushroom escapes US regulation" 532 : 293-, 2016

77 Shen B, "Expression of ZmLEC1 and ZmWRI1increases seed oil production in maize" 153 : 980-987, 2010

78 Zhou X, "Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy" 208 : 298-301, 2015

79 Makarova KS, "Evolution and classification of the CRISPR-Cas systems" 9 : 467-477, 2011

80 Perez EE, "Establishment of HIV-1 resistance in CD41 T cells by genome editing using zinc-finger nucleases" 26 : 808-816, 2008

81 Ji X, "Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants" 1 : 15144-, 2015

82 Center_for_Food_Safety, "Environmental, Farmer, and Consumer Groups Demand Higher Standards for Genetically Engineered (GE)Crop Regulations"

83 Wang F, "Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922" 11 : e0154027-, 2016

84 Arnould S, "Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells" 371 : 49-65, 2007

85 Hou Z, "Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis" 110 : 15644-15649, 2013

86 Brooks C, "Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated 9 system" 166 : 1292-1297, 2014

87 Cermak T, "Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting" 39 : e82-, 2011

88 Fan D, "Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation" 5 : 12217-, 2015

89 Chevalier BS, "Design, activity, and structure of a highly specific artificial endonuclease" 10 : 895-905, 2002

90 Jiang W, "Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice" 41 : e188-, 2013

91 Kraft K, "Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice" 10 : 833-839, 2015

92 Woo JW, "DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins" 33 : 1162-1164, 2015

93 Wyman C, "DNA double-strand break repair: all’s well that ends well" 40 : 363-383, 2006

94 Davis AJ, "DNA double strand break repair via non-homologous end-joining" 2 : 130-143, 2013

95 Shan Q, "Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology" 13 : 791-800, 2015

96 The Council of the European Communities, "Council Directive 90/220/ EEC of 23 April 1990 on the deliberate release into the environment of genetically modified organisms" 117 : 15-27, 1990

97 Araki M, "Consumer acceptance of food crops developed by genome editing" 35 : 1507-1518, 2016

98 Brunet E, "Chromosomal translocations induced at specified loci in human stem cells" 106 : 10620-10625, 2009

99 Ali Z, "CRISPR/Cas9-mediated viral interference in plants" 16 : 238-, 2015

100 Gao J, "CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum" 87 : 99-110, 2015

101 van Nocker S, "Breeding better cultivars, faster:applications of new technologies for the rapid deployment of superior horticultural tree crops" 1 : 14022-, 2014

102 Boch J, "Breaking the code of DNA binding specificity of TAL-type III effectors" 326 : 1509-1512, 2009

103 Endo M, "Biallelic gene targeting in rice" 170 : 667-677, 2016

104 Gao Y, "Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development" 112 : 2275-2280, 2015

105 Cho SW, "Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases" 24 : 132-141, 2014

106 Miller JC, "An improved zinc-finger nuclease architecture for highly specific genome editing" 25 : 778-785, 2007

107 Jinek M, "A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity" 337 : 816-821, 2012

108 Epinat JC, "A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells" 31 : 2952-2962, 2003

109 Mussolino C, "A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity" 39 : 9283-9293, 2011

110 Abiri R, "A critical review of the concept of transgenic plants: insights into pharmaceutical biotechnology and molecular farming" 18 : 21-42, 2015

111 Albert NW, "A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots" 26 : 962-980, 2014