Towards mastering CRISPR-induced gene knock-in in plants: Survey of key features and focus on the model Physcomitrella patens

Bortesi, 2015, The CRISPR/Cas9 system for plant genome editing and beyond, Biotechnol. Adv., 33, 41, 10.1016/j.biotechadv.2014.12.006 Shi, 2016, ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions, Plant Biotechnol. J. Li, 2016, Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9, Nat. Plants, 2, 16139, 10.1038/nplants.2016.139 Sadhu, 2016, CRISPR-directed mitotic recombination enables genetic mapping without crosses, Science, 352, 1113, 10.1126/science.aaf5124 Piatek, 2015, RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors, Plant Biotechnol. J., 13, 578, 10.1111/pbi.12284 Svitashev, 2015, Targeted Mutagenesis, Precise Gene Editing, and Site-Specific Gene Insertion in Maize Using Cas9 and Guide RNA, Plant Physiol., 169, 931, 10.1104/pp.15.00793 Ren, 2016, CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.), Sci. Rep., 6, 1, 10.1038/srep32289 Čermák, 2015, High-frequency, precise modification of the tomato genome, Genome Biol., 16, 232, 10.1186/s13059-015-0796-9 Li, 2016, Development of japonica Photo-Sensitive Genic Male Sterile Rice Lines by Editing Carbon Starved Anther Using CRISPR/Cas9, J. Genet. Genomics, 43, 415, 10.1016/j.jgg.2016.04.011 Schiml, 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, 10.1111/tpj.12704 Shan, 2014, Genome editing in rice and wheat using the CRISPR/Cas system, Nat. Protoc., 9, 2395, 10.1038/nprot.2014.157 Jiang, 2013, Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice, Nucleic Acids Res., 41, 10.1093/nar/gkt780 Wang, 2014, Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew, Nat. Biotechnol., 32, 947, 10.1038/nbt.2969 Chandrasekaran, 2016, Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology, Mol. Plant Pathol., 17, 1140, 10.1111/mpp.12375 Ito, 2015, CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening, Biochem. Biophys. Res. Commun., 467, 76, 10.1016/j.bbrc.2015.09.117 Li, 2016, Reassessment of the Four Yield-related Genes Gn1a, DEP1, GS3, and IPA1 in Rice Using a CRISPR/Cas9 System., Front, Plant Sci., 7, 377 Xu, 2016, Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice, J. Genet. Genomics, 43, 529, 10.1016/j.jgg.2016.07.003 Sovová, 2016, Genome editing with engineered nucleases in economically important animals and plants: state of the art in the research pipeline, Curr. Issues Mol. Biol., 21, 41 Lawrenson, 2015, Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease, Genome Biol., 1 Li, 2014, The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte, Plant Cell, 26, 195, 10.1105/tpc.113.116491 Lowe, 2016, Morphogenic Regulators Baby boom and Wuschel Improve Monocot Transformation, Plant Cell, 28, 1998, 10.1105/tpc.16.00124 Iwase, 2015, WIND1-based acquisition of regeneration competency in Arabidopsis and rapeseed, J. Plant. Res., 128, 389, 10.1007/s10265-015-0714-y Mayavan, 2015, Agrobacterium-mediated in planta genetic transformation of sugarcane setts, Plant Cell Rep., 34, 1835, 10.1007/s00299-015-1831-8 Subramanyam, 2013, Contributions of the RAD51 N-terminal domain to BRCA2-RAD51 interaction, Nucleic Acids Res., 41, 9020, 10.1093/nar/gkt691 Morineau, 2016, Selective gene dosage by CRISPR-Cas9 genome editing in hexaploid Camelina sativa, Plant Biotechnol. J. Feng, 2014, Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis, Proc. Natl. Acad. Sci., 111, 4632, 10.1073/pnas.1400822111 Butler, 2016, Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases, Front. Plant Sci., 7, 1, 10.3389/fpls.2016.01045 Terada, 2002, Efficient gene targeting by homologous recombination in rice, Nat. Biotechnol., 20, 1030, 10.1038/nbt737 Shimatani, 2015, Positive-negative-selection-mediated gene targeting in rice, Front. Plant Sci., 5, 1, 10.3389/fpls.2014.00748 Hahn, 2017, An efficient visual screen for CRISPR/Cas9 activity in Arabidopsis thaliana, Front. Plant Sci., 8, 39, 10.3389/fpls.2017.00039 Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 Haeussler, 2016, Genome Editing with CRISPR-Cas9: Can It Get Any Better?, J. Genet. Genomics, 43, 239, 10.1016/j.jgg.2016.04.008 Dang, 2015, Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency, Genome Biol., 16, 280, 10.1186/s13059-015-0846-3 R. Xu, R. Qin, H. Li, D. Li, L. Li, P. Wei, J. Yang, Generation of targeted mutant rice using a CRISPR-Cpf1 system., Plant Biotechnol. J. (2016) in press, DOI: 10.1111/pbi.12669. doi:10.1111/pbi.12669. Sternberg, 2015, Conformational control of DNA target cleavage by CRISPR-Cas9, Nature, 527, 1, 10.1038/nature15544 Xu, 2015, Sequence determinants of improved CRISPR sgRNA design, Genome Res., 25, 1147, 10.1101/gr.191452.115 Wong, 2015, WU-CRISPR: characteristics of functional guide RNAs for the CRISPR/Cas9 system, Genome Biol., 16, 218, 10.1186/s13059-015-0784-0 Ding, 2016, Recent advances in genome editing using CRISPR/Cas9, Front. Plant Sci., 7, 703, 10.3389/fpls.2016.00703 Ren, 2014, Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila, Cell Rep., 9, 1151, 10.1016/j.celrep.2014.09.044 Farboud, 2015, Dramatic enhancement of genome editing by CRISPR/Cas9 through improved guide RNA design, Genetics, 199, 959, 10.1534/genetics.115.175166 Collonnier, 2016, CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens, Plant Biotechnol. J., 1 Miao, 2013, Targeted mutagenesis in rice using CRISPR-Cas system, Cell Res., 23, 1233, 10.1038/cr.2013.123 Shan, 2013, Targeted genome modification of crop plants using a CRISPR-Cas system, Nat. Biotechnol., 31, 686, 10.1038/nbt.2650 Fauser, 2014, Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana, Plant J., 79, 348, 10.1111/tpj.12554 He, 2016, Knock-in of large reporter genes in human cells via CRISPR/Cas9-induced homology-dependent and independent DNA repair, Nucleic Acids Res., 44, 10.1093/nar/gkw064 Komor, 2016, Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage, Nature, 61, 5985 Y. Zong, Y. Wang, C. Li, R. Zhang, K. Chen, Y. Ran, J. Qiu, D. Wang, C. Gao, Precise base editing in rice, wheat and maize with a Cas9- cytidine deaminase fusion, (2017) 4–7. doi:10.1038/nbt.3811. Li, 2016, Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system, Mol. Plant., 526 Lu, 2016, Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system, Mol. Plant., 523 Shimatani, 2017, Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion, Nat. Biotechnol., 3 Komor, 2016, CRISPR-based technologies for the manipulation of eukaryotic genomes, Cell, 168, 1 Steinert, 2015, Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus, Plant J., 84, 1295, 10.1111/tpj.13078 Wright, 2016, Biology and applications of CRISPR systems: harnessing nature’s toolbox for genome engineering, Cell, 164, 29, 10.1016/j.cell.2015.12.035 Shmakov, 2015, Discovery and functional characterization of diverse class 2 CRISPR-Cas systems, Mol. Cell, 60, 385, 10.1016/j.molcel.2015.10.008 Fonfara, 2016, The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA, Nature, 532, 517, 10.1038/nature17945 Hu, 2016, Targeted mutagenesis in rice using CRISPR-Cpf1 system, J. Genet. Genomics, 44, 2016 Kim, 2017, CRISPR/Cpf1-mediated DNA-free plant genome editing, Nat. Commun., 8, 14406, 10.1038/ncomms14406 Tang, 2017, A CRISPR–Cpf1 system for efficient genome editing and transcriptional repression in plants, Nat. Plants., 3, 17018, 10.1038/nplants.2017.18 Endo, 2016, Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida, Sci. Rep., 6, 38169, 10.1038/srep38169 Gao, 2016, DNA-guided genome editing using the Natronobacterium gregoryi Argonaute, Nat. Biotechnol., 34, 768, 10.1038/nbt.3547 Wang, 2016, Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus Using CRISPR-Cas9, Front. Plant Sci., 7, 1333 Yan, 2015, High-efficiency genome editing in arabidopsis using YAO promoter-driven CRISPR/Cas9 system, Mol. Plant, 8, 1820, 10.1016/j.molp.2015.10.004 Mao, 2016, Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis, Plant Biotechnol. J., 14, 519, 10.1111/pbi.12468 Schiml, 2016, Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas, Plant Methods, 12, 8, 10.1186/s13007-016-0103-0 Chu, 2015, Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells, Nat. Biotechnol., 33, 543, 10.1038/nbt.3198 Sakuma, 2015, MMEJ-assisted gene knock-in using TALENs and CRISPR-Cas9 with the PITCh systems, Nat. Protoc., 11, 118, 10.1038/nprot.2015.140 Sun, 2016, Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase, Mol. Plant, 9, 628, 10.1016/j.molp.2016.01.001 Butler, 2015, Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas system, PLoS One, 10, e0144591, 10.1371/journal.pone.0144591 Li, 2013, Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems, Nat. Biotechnol., 31, 684, 10.1038/nbt.2652 Richardson, 2016, Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA, Nat. Biotechnol., 34, 339, 10.1038/nbt.3481 Liang, 2017, Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA, J. Biotechnol., 241, 136, 10.1016/j.jbiotec.2016.11.011 Renaud, 2016, Improved genome editing efficiency and flexibility using modified oligonucleotides with TALEN and CRISPR-Cas9 nucleases, Cell Rep., 14, 2263, 10.1016/j.celrep.2016.02.018 Zhang, 2016, Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA, Nat. Commun., 7, 12617, 10.1038/ncomms12617 Woo, 2015, DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins, Nat. Biotechnol., 33, 1162, 10.1038/nbt.3389 Svitashev, 2016, Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes, Nat. Commun., 7, 13274, 10.1038/ncomms13274 Subburaj, 2016, Site-directed mutagenesis in Petunia×hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins, Plant Cell Rep., 35, 1535, 10.1007/s00299-016-1937-7 Engler, 2008, A one pot, one step, precision cloning method with high throughput capability, PLoS One, 3, 10.1371/journal.pone.0003647 Gibson, 2009, Enzymatic assembly of DNA molecules up to several hundred kilobases, Nat. Methods, 6, 343, 10.1038/nmeth.1318 Liang, 2016, Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing, Sci. Rep., 6, 21451, 10.1038/srep21451 Vad-Nielsen, 2016, Golden gate assembly of CRISPR gRNA expression array for simultaneously targeting multiple genes, Cell. Mol. Life Sci., 73, 4315, 10.1007/s00018-016-2271-5 Vazquez-Vilar, 2016, A modular toolbox for gRNA–Cas9 genome engineering in plants based on the GoldenBraid standard, Plant Methods, 12, 10, 10.1186/s13007-016-0101-2 Parry, 2016, Meeting report: GARNet/OpenPlant CRISPR-Cas workshop, Plant Methods., 12, 6, 10.1186/s13007-016-0104-z Lowder, 2015, A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation, Plant Physiol., 169, 971, 10.1104/pp.15.00636 Tang, 2016, A single transcript CRISPR-Cas9 system for efficient genome editing in plants, Mol. Plant, 9, 1088, 10.1016/j.molp.2016.05.001 Xie, 2015, Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system, Proc. Natl. Acad. Sci. U.S.A., 112, 3570, 10.1073/pnas.1420294112 W. Wang, A. Akhunova, S. Chao, E. Akhunov, Optimizing multiplex CRISPR/CAS9Cas9 system for wheat genome editing, Submitted. (2016). doi:10.1101/051342. Nissim, 2014, Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells, Mol. Cell, 54, 698, 10.1016/j.molcel.2014.04.022 Osakabe, 2016, Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants, Sci. Rep., 6, 26685, 10.1038/srep26685 Baltes, 2015, Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system, Nat. Plants, 1, 15145, 10.1038/nplants.2015.145 Yin, 2015, A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing, Sci. Rep., 5, 14926, 10.1038/srep14926 Larsen, 2012, RNA viral vectors for improved Agrobacterium -mediated transient expression of heterologous proteins in Nicotiana benthamiana cell suspensions and hairy roots, BMC Biotechnol., 12, 1, 10.1186/1472-6750-12-21 Alagoz, 2016, Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology, Nat. Publ. Gr., 1 Baltes, 2014, DNA replicons for plant genome engineering, Plant Cell, 26, 151, 10.1105/tpc.113.119792 Gil-Humanes, 2017, High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9, Plant J., 89, 1251, 10.1111/tpj.13446 Malnoy, 2016, DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins, Front. Plant Sci., 7, 1, 10.3389/fpls.2016.01904 Liang, 2017, ARTICLE Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes, Nat. Publ. Gr., 8, 1 Burstein, 2016, New CRISPR-Cas systems from uncultivated microbes, Nature, 1 Pierce, 2001, Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells, Genes Dev., 15, 3237, 10.1101/gad.946401 Delacôte, 2002, An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells, Nucleic Acids Res., 30, 3454, 10.1093/nar/gkf452 Qi, 2013, Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways, Genome Res., 23, 547, 10.1101/gr.145557.112 Gutschner, 2016, Post-translational regulation of Cas9 during G1 enhances homology-directed repair, Cell Rep., 14, 1555, 10.1016/j.celrep.2016.01.019 Howden, 2016, A Cas9 variant for efficient generation of indel-free knockin or gene-corrected human pluripotent stem cells, Stem Cell Rep., 7, 508, 10.1016/j.stemcr.2016.07.001 Saintigny, 2007, XRCC4 in G1 suppresses homologous recombination in S/G2, in G1 checkpoint-defective cells, Oncogene, 26, 2769, 10.1038/sj.onc.1210075 Saleh-Gohari, 2004, Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells, Nucleic Acids Res., 32, 3683, 10.1093/nar/gkh703 Maruyama, 2015, Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining, Nat. Biotechnol., 33, 538, 10.1038/nbt.3190 Song, 2016, RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency, Nat. Commun., 7, 10548, 10.1038/ncomms10548 Yu, 2015, Small molecules enhance CRISPR genome editing in pluripotent stem cells, Cell Stem Cell, 16, 142, 10.1016/j.stem.2015.01.003 Hanin, 2003, Plant genome modification by homologous recombination, Curr. Opin. Plant Biol., 6, 157, 10.1016/S1369-5266(03)00016-5 Schaefer, 2002, A new moss genetics: targeted mutagenesis in Physcomitrella patens, Annu. Rev. Plant Biol., 53, 477, 10.1146/annurev.arplant.53.100301.135202 M. Lopez-Obando, B. Hoffmann, C. Géry, A. Guyon-Debast, E. Téoulé, C. Rameau, S. Bonhomme, F. Nogué, Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens, G3 (Bethesda). (2016) 1–27. doi:10.1534/g3.116.033266. Trouiller, 2006, MSH2 is essential for the preservation of genome integrity and prevents homeologous recombination in the moss Physcomitrella patens, Nucleic Acids Res., 34, 232, 10.1093/nar/gkj423 Kamisugi, 2012, MRE11 and RAD50, but not NBS1, are essential for gene targeting in the moss Physcomitrella patens, Nucleic Acids Res., 40, 3496, 10.1093/nar/gkr1272 Schaefer, 2010, RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens, DNA Repair (Amst), 9, 526, 10.1016/j.dnarep.2010.02.001 Trouiller, 2007, Comparison of gene targeting efficiencies in two mosses suggests that it is a conserved feature of Bryophyte transformation, Biotechnol. Lett., 29, 1591, 10.1007/s10529-007-9423-5 Puchta, 2013, Gene targeting in plants: 25 years later, Int. J. Dev. Biol., 57, 629, 10.1387/ijdb.130194hp Kamisugi, 2006, The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration, Nucleic Acids Res., 34, 6205, 10.1093/nar/gkl832 Schaefer, 1997, Efficient gene targeting in the moss Physcomitrella patens, Plant J., 11, 1195, 10.1046/j.1365-313X.1997.11061195.x Charlot, 2014, RAD51B plays an essential role during somatic and meiotic recombination in Physcomitrella, Nucleic Acids Res., 42, 11965, 10.1093/nar/gku890 Waltz, 2016, CRISPR-edited crops free to enter market, skip regulation, Nat. Biotechnol., 34, 10.1038/nbt0616-582 Mali, 2013, RNA-guided human genome engineering via Cas9, Science, 339, 823, 10.1126/science.1232033 Ashton, 1977, The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens, Mol. Gen. Genet. MGG., 154, 87, 10.1007/BF00265581