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Plant DNA Repair Pathways and Their Applications in Genome Engineering

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Plant Genome Editing with CRISPR Systems

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1917))

Abstract

Remarkable progress in the development of technologies for sequence-specific modification of primary DNA sequences has enabled the precise engineering of crops with novel characteristics. These programmable sequence-specific modifiers include site-directed nucleases (SDNs) and base editors (BEs). Currently, these genome editing machineries can be targeted to specific chromosomal locations to induce sequence changes. However, the sequence mutation outcomes are often greatly influenced by the type of DNA damage being generated, the status of host DNA repair machinery, and the presence and structure of DNA repair donor molecule. The outcome of sequence modification from repair of DNA double-strand breaks (DSBs) is often uncontrollable, resulting in unpredictable sequence insertions or deletions of various sizes. For base editing, the precision of intended edits is much higher, but the efficiency can vary greatly depending on the type of BE used or the activity of the endogenous DNA repair systems. This article will briefly review the possible DNA repair pathways present in the plant cells commonly used for generating edited variants for genome engineering applications. We will discuss the potential use of DNA repair mechanisms for developing and improving methodologies to enhance genome engineering efficiency and to direct DNA repair processes toward the desired outcomes.

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References

  1. Britt AB (2004) Repair of DNA damage induced by solar UV. Photosynth Res 81:105–112

    Article  CAS  Google Scholar 

  2. Spampinato CP (2017) Protecting DNA from errors and damage: an overview of DNA repair mechanisms in plants compared to mammals. Cell Mol Life Sci 74:1693–1709

    Article  CAS  PubMed  Google Scholar 

  3. Manova V, Gruszka D (2015) DNA damage and repair in plants-from models to crops. Front Plant Sci 6:885

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hu Z, Cools T, De Veylder L (2016) Mechanisms used by plants to cope with DNA damage. Annu Rev Plant Biol 67:439–462

    Article  CAS  PubMed  Google Scholar 

  5. Ueda T, Nakamura C (2011) Ultraviolet-defense mechanisms in higher plants. Biotechnol Biotechnol Equip 25:2177–2182

    Article  CAS  Google Scholar 

  6. Schärer OD (2013) Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol 5:a012609

    Article  PubMed  PubMed Central  Google Scholar 

  7. Alekseev S, Coin F (2015) Orchestral maneuvers at the damaged sites in nucleotide excision repair. Cell Mol Life Sci 72:2177–2186

    Article  CAS  PubMed  Google Scholar 

  8. Krokan HE, Bjoras M (2013) Base excision repair. Cold Spring Harb Perspect Biol 5:a012583

    Article  PubMed  PubMed Central  Google Scholar 

  9. Crouse GF (2016) Non-canonical actions of mismatch repair. DNA Repair 38:102–109

    Article  CAS  PubMed  Google Scholar 

  10. Kunkel T, Erie D (2015) Eukaryotic mismatch repair in relation to DNA replication. Annu Rev Genet 49:291–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Caldecott KW (2008) Single-strand break repair and genetic disease. Nat Rev Genet 9:619–631

    Article  CAS  PubMed  Google Scholar 

  12. Caldecott KW (2014) DNA single-strand break repair. Exp Cell Res 329:2–8

    Article  CAS  PubMed  Google Scholar 

  13. Gorbunova V, Levy AA (1999) How plants make ends meet: DNA double-strand break repair. Trends Plant Sci 4:263–269

    Article  CAS  PubMed  Google Scholar 

  14. Deriano L, Roth DB (2013) Modernizing the nonhomologous end-joining repertoire: Alternative and classical NHEJ share the stage. Annu Rev Genet 47:433–455

    Article  CAS  PubMed  Google Scholar 

  15. Roth N, Klimesch J, Dukowic-Schulze S et al (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

    Article  CAS  PubMed  Google Scholar 

  16. Chang HHY, Pannunzio NR, Adachi N et al (2017) Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol 18:495–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chatterjee N, Walker GC (2017) Mechanisms of DNA damage, repair, and mutagenesis. Environ Mol Mutagen 58:235–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hustedt N, Durocher D (2017) The control of DNA repair by the cell cycle. Nat Cell Biol 19:1–9

    Article  CAS  Google Scholar 

  19. Puchta H, Fauser F (2014) Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J 78:727–741

    Article  CAS  PubMed  Google Scholar 

  20. Faraji S, Dreuw A (2017) Insights into light-driven DNA repair by photolyases: challenges and opportunities for electronic structure theory. Photochem Photobiol 93:37–50

    Article  CAS  PubMed  Google Scholar 

  21. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marin MI et al (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci U S A 103:6853–6858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Abbotts R, Wilson DM III (2017) Coordination of DNA single strand break repair. Free Radic Biol Med 107:228–244

    Article  CAS  PubMed  Google Scholar 

  23. Fauser F, Schiml S, Puchta H (2014) Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J 79:348–359

    Article  CAS  PubMed  Google Scholar 

  24. Davis L, Maizels N (2016) Two direct pathways support gene correction by single-stranded donors at DNA nicks. Cell Rep 17:1872–1881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kan Y, Ruis B, Takasugi T et al (2017) Mechanisms of precise genome editing using oligonucleotide donors. Genome Res 27:1099–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Komor AC, Kim YB, Packer MS (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14

    CAS  PubMed  Google Scholar 

  28. Ceccaldi R, Rondinelli B, D’Andrea AD (2016) Repair pathway choices and consequences at the double-strand break. Trends Cell Biol 26:52–64

    Article  CAS  PubMed  Google Scholar 

  29. Steinert J, Schiml S, Puchta H (2016) Homology-based double-strand break-induced genome engineering in plants. Plant Cell Rep 35:1429–1438

    Article  CAS  PubMed  Google Scholar 

  30. Verma P, Greeberg RA (2017) Noncanonical views of homology-directed DNA repair. Genes Dev 30:1138–1154

    Article  Google Scholar 

  31. Longhese MP, Bonetti D, Guerini I et al (2009) DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair 8:1127–1138

    Article  CAS  PubMed  Google Scholar 

  32. Lambing C, Franklin FCH, Wang C-JR (2017) Understanding and manipulating meiotic recombination in plants. Plant Physiol 173:1530–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Choi K, Zhou X, Kelly KA et al (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoter. Nat Genet 45:1327–1336

    Article  CAS  PubMed  Google Scholar 

  34. Knoll A, Higgins JD, Seeliger K et al (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24:1448–1464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gallego ME, Jeanneau M, Granier F et al (2001) Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J 25:31–41

    CAS  PubMed  Google Scholar 

  36. Puizina J, Siroky J, Mokros P et al (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Aklilu BB, Sonderquist RS, Culligan KM (2014) Genetic analysis of the replication protein A large subunit family in Arabidopsis reveals unique and overlapping roles in DNA repair, meiosis and DNA replication. Nucleic Acids Res 42:3104–3118

    Article  CAS  PubMed  Google Scholar 

  38. Karanam K, Kafri R, Loewer A et al (2012) Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in mid S phase. Mol Cell 47:320–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Troung LN, Li Y, Shi LZ et al (2013) Microhomology mediated end joining and homologous recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc Natl Acad Sci U S A 110:7720–7725

    Article  Google Scholar 

  40. Kovalchuk I, Kovalchuk O, Kalck V et al (2003) Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:760–762

    Article  CAS  PubMed  Google Scholar 

  41. LeBlanc C, Zhang F, Mendez J et al (2018) Increased efficiency of targeted mutagenesis by CRISPR/Cas9 in plants using heat stress. Plant J 93:377–386

    Article  CAS  PubMed  Google Scholar 

  42. Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17:6086–6095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zetsche B, Gootenberg JS, Abudayyeh OO et al (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:1–13

    Article  Google Scholar 

  44. Tang X, Lowder LG, Zhang T et al (2017) A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants 3:17018

    Article  CAS  PubMed  Google Scholar 

  45. Li T, Liu B, Spalding MH et al (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392

    Article  CAS  PubMed  Google Scholar 

  46. Lloyd AH, Wang D, Timmis JN (2012) Single molecule PCR reveals similar patterns of non-homologous DSB repair in tobacco and Arabidopsis. PLoS One 7:e32255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kirik A, Salomon S, Puchta H (2000) Species-specific double-strand break repair and genome evolution in plants. EMBO J 19:5562–5566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Feng Z, Mao Y, Xu N et al (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci U S A 111:4632–4637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Miyaoka Y, Berman JR, Cooper SB et al (2016) Systematic quantification of HDR and NHEJ reveals effects of locus, nuclease, and cell type on genome-editing. Sci Rep 6:23549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Vu GTH, Cao HX, Fauser F et al (2017a) Endogenous sequence patterns predispose the repair modes of CRISPR/Cas9-induced DNA double-stranded breaks in Arabidopsis thaliana. Plant J 92:57–67

    Article  CAS  PubMed  Google Scholar 

  51. Vu GTH, Cao HX, Reiss B et al (2017b) Deletion bias in DNA double-strand break repair differentially contributes to plant genome shrinkage. New Phytol 214:1712–1721

    Article  CAS  PubMed  Google Scholar 

  52. Gil-Humanes J, Wang Y, Liang Z et al (2017) High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J 89:1251–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Liang Z, Zhang K, Chen K et al (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas systems. J Genet Genomics 41:63–68

    Article  CAS  PubMed  Google Scholar 

  54. Marton I, Zuker A, Shklarman E et al (2010) Nontransgenic genome modification in plant cells. Plant Physiol 154:1079–1087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc-finger nucleases. Proc Natl Acad Sci U S A 107:12034–12039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lloyd A, Plaisier CL, Carroll D et al (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci U S A 102:2232–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Charbonnel C, Allain E, Gallego ME et al (2011) Kinetic analysis of DNA double-strand break repair pathways in Arabidopsis. DNA Repair 10:611–619

    Article  CAS  PubMed  Google Scholar 

  58. Richardson CD, Ray GJ, DeWitt MA et al (2016) Enhancing homology-dependent gene editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat Biotechnol 34:339–344

    Article  CAS  PubMed  Google Scholar 

  59. Schiml S, Fauser F, Puchta H (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80:1139–1150

    Article  CAS  PubMed  Google Scholar 

  60. Schiml S, Fauser F, Puchta H (2016) Repair of adjacent single-strand breaks is often accompanied by the formation of tandem sequence duplications in plant genome. Proc Natl Acad Sci U S A 113:7266–7271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Qi Y, Zhang Y, Zhang F et al (2013) Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways. Genome Res 23:547–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Nishizawa-Yokoi A, Cermak T, Hoshino T et al (2016) A defect in DNA ligase4 enhances the frequency of TALEN-mediated targeted mutagenesis in rice. Plant Physiol 170:653–666

    Article  CAS  PubMed  Google Scholar 

  63. van Kregten M, de Pater S, Romeijn R et al (2016) T-DNA integration in plants results from polymerase-θ-mediated DNA repair. Nat Plants 2:16164

    Article  PubMed  Google Scholar 

  64. Chilton MD, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133:956–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Orlando SJ, Santiago Y, DeKelver RC et al (2010) Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology. Nucleic Acid Res 38:e152

    Article  PubMed  PubMed Central  Google Scholar 

  66. Auer TO, Duroure K, De Cian A et al (2014) Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res 24:142–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Nakade S, Tsubota T, Sakane Y et al (2014) Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun 5:5560

    Article  CAS  PubMed  Google Scholar 

  68. Li J, Meng X, Zong Y et al (2016) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2:16139

    Article  CAS  PubMed  Google Scholar 

  69. Suzuki K, Tsunekawa Y, Hernandez-Benitez R et al (2016) In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration. Nature 540:144–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Cristea S, Freyvert Y, Santiago Y et al (2013) In vivo cleavage of transgene donors promotes nuclease-mediated targeted integration. Botechnol Bioeng 110:871–880

    Article  CAS  Google Scholar 

  71. Sauer NJ, Narváez-Vásquez J, Mozoruk J et al (2016) Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol 170:1917–1928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Shan Q, Wang Y, Li J et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas9 system. Nat Biotechnol 31:686–688

    Article  CAS  PubMed  Google Scholar 

  73. Svitashev S, Young JK, Schwartz C et al (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–945

    Article  PubMed  PubMed Central  Google Scholar 

  74. Paix A, Folkmann A, Goldman DH et al (2017) Precision genome editing using synthesis-dependent repair of Cas9-induced DNA breaks. Proc Natl Acad Sci U S A 114:E10745–E10754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Canny MD, Moatti N, Wan LCK et al (2018) Inhibition of 53BP1 favors homology-dependent DNA repair and increases CRISPR-Cas9 genome-editing efficiency. Nat Biotechnol 36:95–102

    Article  CAS  PubMed  Google Scholar 

  76. Quadros RM, Miura H, Harms DW et al (2017) Easi-CRISPR: a robust method for one-step generation of mice carrying conditional and insertion alleles using long ssDNA donors and CRISPR ribonucleoproteins. Genome Biol 18:92

    Article  PubMed  PubMed Central  Google Scholar 

  77. Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci U S A 93:5055–5060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Shukla VK, Doyon Y, Miller JC et al (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441

    Article  CAS  PubMed  Google Scholar 

  79. Shi J, Gao H, Wang H et al (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216

    Article  CAS  PubMed  Google Scholar 

  80. D’Halluin K, Vanderstraeten C, Stals E et al (2008) Homologous recombination: a basis for targeted genome optimization in crop species such as maize. Plant Biotechnol J 6:93–102

    PubMed  Google Scholar 

  81. Baltes NJ, Gil-Humanes J, Cermak T et al (2014) DNA replicons for plant genome engineering. Plant Cell 26:151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Čermák T, Baltes NJ, Čegan R et al (2015) High-frequency, precise modification of the tomato genome. Genome Biol 16:232

    Article  PubMed  PubMed Central  Google Scholar 

  83. Chu VT, Weber T, Wefers B et al (2015) Increasing the efficiency of homology-dependent repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat Biotechnol 33:543–548

    Article  CAS  PubMed  Google Scholar 

  84. Maruyama T, Dougan SK, Truttmann MC et al (2015) Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol 33:538–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gherbi H, Gallego ME, Jalut N et al (2001) Homologous recombination in planta is stimulated in the absence of Rad50. EMBO Rep 2:287–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Endo M, Ishikawa Y, Osakabe K et al (2006) Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J 25:5443–5634

    Article  Google Scholar 

  87. Hanin M, Mengiste T, Bogucki A et al (2000) Elevated levels of intrachromosomal homologous recombination in Arabidopsis overexpressing the MIM gene. Plant J 24:183–189

    Article  CAS  PubMed  Google Scholar 

  88. Nishida KN, Arazoe T, Yachie N et al (2016) Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:aaf8729

    Article  PubMed  Google Scholar 

  89. Komor AC, Zhao KT, Packer MS et al (2017) Improved base excision repair inhibition and bacteriophage Mu Gam protein yields C:G-to-T:A base editors with higher efficiency and product purity. Sci Adv 3:eaao4774

    Article  PubMed  PubMed Central  Google Scholar 

  90. Gaudelli NM, Komor AC, Rees HA et al (2017) Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage. Nature 551:464–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kim YB, Komor AC, Levy JM et al (2017) Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol 35:371–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Hess GT, Fresard L, Han K et al (2016) Direct evolution using dCas9-targted somatic hypermutation in mammalian cells. Nat Methods 13:1036–1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Chaudhuri J et al (2003) Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422:726–730

    Article  CAS  PubMed  Google Scholar 

  94. Li J, Sun Y, Du J et al (2016) Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol Plant 10:526–529

    Article  PubMed  Google Scholar 

  95. Lu Y, Zhu JK (2016) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10:523–525

    Article  PubMed  Google Scholar 

  96. Zong Y, Wang Y, Li C et al (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35(5):438–440. https://doi.org/10.1038/nbt.3811

    Article  CAS  PubMed  Google Scholar 

  97. 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 35:441–443

    Article  CAS  PubMed  Google Scholar 

  98. Ren B, Yan F, Kuang Y et al (2018) Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant. Mol Plant 11(4):623–626. https://doi.org/10.1016/j.molp.2018.01.005

    Article  CAS  PubMed  Google Scholar 

  99. Hua K, Tao X, Yuan F et al (2018) Precise A·T to G·C base editing in the rice genome. Mol Plant 11(4):627–630. https://doi.org/10.1016/j.molp.2018.02.007

    Article  CAS  PubMed  Google Scholar 

  100. Yan F, Kuang Y, Ren B et al (2018) High-efficient A·T to G·C base editing by Cas9n-guided tRNA adenosine deaminase in rice. Mol Plant 11(4):631–634. https://doi.org/10.1016/j.molp.2018.02.008

    Article  CAS  PubMed  Google Scholar 

  101. Wang Y, Cheng X, Shan Q et al (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951

    Article  CAS  PubMed  Google Scholar 

  102. Clasen BM, Stoddard TJ, Luo S et al (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176

    Article  CAS  PubMed  Google Scholar 

  103. Zhang Y, Liang Z, Zong Y et al (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Woo JW, Kim J, Kwon SI et al (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164

    Article  CAS  PubMed  Google Scholar 

  105. Svitashev S, Schwartz C, Lenders B et al (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun 7:13275

    Article  Google Scholar 

  106. Liang Z, Chen LT et al (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:14261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Lv W, Du B, Shangguan X et al (2014) BAC and RNA sequencing reveal the brown planthopper resistance gene BPH15 in a recombination cold spot that mediates a unique defense mechanism. BMC Genomics 15:674

    Article  PubMed  PubMed Central  Google Scholar 

  108. Bernardo R (2017) Prospective targeted recombination and genetic gains for quantitative traits in maize. Plant Genome 10:1–9

    Article  CAS  Google Scholar 

  109. Sarno R, Vicq Y, Uematsu N et al (2017) Programming sites of meiotic crossovers using Spo11 fusion proteins. Nucleic Acids Res 45:e164

    Article  PubMed  PubMed Central  Google Scholar 

  110. Sanchez-Leon S, Gil-Humanes J, Ozuna CV et al (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16(4):902–910. https://doi.org/10.1111/pbi.12837

    Article  CAS  PubMed  Google Scholar 

  111. LeKomtsev S, Aligianni S, Lapao A et al (2016) Efficient generation and reversion of chromosomal translocations using CRISPR/Cas technology. BMC Genomics 17:739

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Seeds Research, Syngenta Crop Protection, LLC, Research Triangle Park, NC, USA

    Qiudeng Que, Zhongying Chen, Tim Kelliher, David Skibbe, Shujie Dong & Mary-Dell Chilton

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  1. Qiudeng Que
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  2. Zhongying Chen
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  3. Tim Kelliher
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  4. David Skibbe
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  6. Mary-Dell Chilton
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Correspondence to Qiudeng Que .

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  1. Department of Plant Science and Landscape Architecture, University of Maryland College Park, College Park, MD, USA

    Yiping Qi

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Que, Q., Chen, Z., Kelliher, T., Skibbe, D., Dong, S., Chilton, MD. (2019). Plant DNA Repair Pathways and Their Applications in Genome Engineering. In: Qi, Y. (eds) Plant Genome Editing with CRISPR Systems. Methods in Molecular Biology, vol 1917. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-8991-1_1

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  • DOI: https://doi.org/10.1007/978-1-4939-8991-1_1

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