[en] Beyond its predominant role in human and animal therapy, the CRISPR-Cas9 system has also become an essential tool for plant research and plant breeding. Agronomic applications rely on the mastery of gene inactivation and gene modification. However, if the knock-out of genes by non-homologous end-joining (NHEJ)-mediated repair of the targeted double-strand breaks (DSBs) induced by the CRISPR-Cas9 system is rather well mastered, the knock-in of genes by homology-driven repair or end-joining remains difficult to perform efficiently in higher plants. In this review, we describe the different approaches that can be tested to improve the efficiency of CRISPR–induced gene modification in plants, which include the use of optimal transformation and regeneration protocols, the design of appropriate guide RNAs and donor templates and the choice of nucleases and means of delivery. We also present what can be done to orient DNA repair pathways in the target cells, and we show how the moss Physcomitrella patens can be used as a model plant to better understand what DNA repair mechanisms are involved, and how this knowledge could eventually be used to define more performant strategies of CRISPR-induced gene knock-in.
Research center :
INRA Versailles, ULiège-GxABT
Disciplines :
Biotechnology
Author, co-author :
Collonnier, Cécile; INRA Centre de Versailles-Grignon, Versailles Cedex, France > Institut Jean-Pierre Bourgin (UMR1318) > Méiose et Recombinaison
Guyon-Debast, Anouchka; INRA Centre de Versailles-Grignon, Versailles Cedex, France > Institut Jean-Pierre Bourgin (UMR1318) > Méiose et Recombinaison
Maclot, François ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs
Mara, Kostlend; INRA Centre de Versailles-Grignon, Versailles Cedex, France > Institut Jean-Pierre Bourgin (UMR1318) > Méiose et Recombinaison
Charlot, Florence; INRA Centre de Versailles-Grignon, Versailles Cedex, France > Institut Jean-Pierre Bourgin (UMR1318) > Méiose et Recombinaison
Nogué, Fabien; INRA Centre de Versailles-Grignon, Versailles Cedex, France > Institut Jean-Pierre Bourgin (UMR1318) > Méiose et Recombinaison
Language :
English
Title :
Towards mastering CRISPR-induced gene knock-in in plants: Survey of key features and focus on the model Physcomitrella patens
Publication date :
15 May 2017
Journal title :
Methods
ISSN :
1046-2023
eISSN :
1095-9130
Publisher :
Elsevier, Atlanta, United States
Volume :
121-122
Pages :
103-117
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
French programme “Investissements d’Avenir” and French National Research Agency through the research project GENIUS ANR‐11‐BTBR‐0001
Bortesi, L., Fischer, R., The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33 (2015), 41–52, 10.1016/j.biotechadv.2014.12.006.
Shi, J., Gao, H., Wang, H., Lafitte, H.R., Archibald, R.L., Yang, M., Hakimi, S.M., Mo, H., Habben, J.E., ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol. J., 2016, 10.1111/pbi.12603.
Li, J., Meng, X., Zong, Y., Chen, K., Zhang, H., Liu, J., Li, J., Gao, C., Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nat. Plants, 2, 2016, 16139, 10.1038/nplants.2016.139.
Čermák, T., Baltes, N.J., Čegan, R., Zhang, Y., Voytas, D.F., High-frequency, precise modification of the tomato genome. Genome Biol., 16, 2015, 232, 10.1186/s13059-015-0796-9.
Li, Q., Zhang, D., Chen, M., Liang, W., Wei, J., Qi, Y., Yuan, Z., Development of japonica Photo-Sensitive Genic Male Sterile Rice Lines by Editing Carbon Starved Anther Using CRISPR/Cas9. J. Genet. Genomics 43 (2016), 415–419, 10.1016/j.jgg.2016.04.011.
Schiml, S., Fauser, F., Puchta, H., 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 (2014), 1139–1150, 10.1111/tpj.12704.
Shan, Q., Wang, Y., Li, J., Gao, C., Genome editing in rice and wheat using the CRISPR/Cas system. Nat. Protoc. 9 (2014), 2395–2410, 10.1038/nprot.2014.157.
Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., Weeks, D.P., Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res., 41, 2013, 10.1093/nar/gkt780 e188–e188.
Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., Qiu, J., Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32 (2014), 947–951, 10.1038/nbt.2969.
Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A., Arazi, T., Gal-On, A., Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17 (2016), 1140–1153, 10.1111/mpp.12375.
Ito, Y., Nishizawa-Yokoi, A., Endo, M., Mikami, M., Toki, S., CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem. Biophys. Res. Commun. 467 (2015), 76–82, 10.1016/j.bbrc.2015.09.117.
Li, M., Li, X., Zhou, Z., Wu, P., Fang, M., Pan, X., Lin, Q., Luo, W., Wu, G., Li, H., Reassessment of the Four Yield-related Genes Gn1a, DEP1, GS3, and IPA1 in Rice Using a CRISPR/Cas9 System., Front. Plant Sci., 7, 2016, 377, 10.3389/fpls.2016.00377.
Xu, R., Yang, Y., Qin, R., Li, H., Qiu, C., Li, L., Wei, P., Yang, J., Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J. Genet. Genomics 43 (2016), 529–532, 10.1016/j.jgg.2016.07.003.
Sovová, T., Kerins, G., Demnerová, K., Ovesná, J., Genome editing with engineered nucleases in economically important animals and plants: state of the art in the research pipeline. Curr. Issues Mol. Biol. 21 (2016), 41–62 http://www.ncbi.nlm.nih.gov/pubmed/27253613.
Lawrenson, T., Shorinola, O., Stacey, N., Li, C., Østergaard, L., Patron, N., Uauy, C., Harwood, W., Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol., 2015, 1–13, 10.1186/s13059-015-0826-7.
Li, H., Soriano, M., Cordewener, J., Muiño, J.M., Riksen, T., Fukuoka, H., Angenent, G.C., Boutilier, K., The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte. Plant Cell 26 (2014), 195–209, 10.1105/tpc.113.116491.
Lowe, K., Wu, E., Wang, N., Hoerster, G., Hastings, C., Cho, M., Scelonge, C., Lenderts, B., Chamberlin, M., Cushatt, J., Wang, L., Ryan, L., Khan, T., Chow-Yiu, J., Hua, W., Yu, M., Banh, J., Bao, Z., Brink, K., Igo, E., Rudrappa, B., Shamseer, P., Bruce, W., Newman, L., Shen, B., Zheng, P., Bidney, D., Falco, C., Register, J., Zhao, Z.-Y., Xu, D., Jones, T., Gordon-Kamm, W., Morphogenic Regulators Baby boom and Wuschel Improve Monocot Transformation. Plant Cell 28 (2016), 1998–2015, 10.1105/tpc.16.00124.
Iwase, A., Mita, K., Nonaka, S., Ikeuchi, M., Koizuka, C., Ohnuma, M., Ezura, H., Imamura, J., Sugimoto, K., WIND1-based acquisition of regeneration competency in Arabidopsis and rapeseed. J. Plant. Res. 128 (2015), 389–397, 10.1007/s10265-015-0714-y.
Mayavan, S., Subramanyam, K., Jaganath, B., Sathish, D., Manickavasagam, M., Ganapathi, A., Agrobacterium-mediated in planta genetic transformation of sugarcane setts. Plant Cell Rep. 34 (2015), 1835–1848, 10.1007/s00299-015-1831-8.
Subramanyam, S., Jones, W.T., Spies, M., Spies, M.A., Contributions of the RAD51 N-terminal domain to BRCA2-RAD51 interaction. Nucleic Acids Res. 41 (2013), 9020–9032, 10.1093/nar/gkt691.
Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D.-L., Wang, Z., Zhang, Z., Zheng, R., Yang, L., Zeng, L., Liu, X., Zhu, J.-K., Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. 111 (2014), 4632–4637, 10.1073/pnas.1400822111.
Butler, N.M., Baltes, N.J., Voytas, D.F., Douches, D.S., Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front. Plant Sci. 7 (2016), 1–13, 10.3389/fpls.2016.01045.
Terada, R., Urawa, H., Inagaki, Y., Tsugane, K., Iida, S., Efficient gene targeting by homologous recombination in rice. Nat. Biotechnol. 20 (2002), 1030–1034, 10.1038/nbt737.
Shimatani, Z., Nishizawa-Yokoi, A., Endo, M., Toki, S., Terada, R., Positive-negative-selection-mediated gene targeting in rice. Front. Plant Sci. 5 (2015), 1–7, 10.3389/fpls.2014.00748.
Hahn, F., Mantegazza, O., Greiner, A., Hegemann, P., Eisenhut, M., Weber, A.P.M., An efficient visual screen for CRISPR/Cas9 activity in Arabidopsis thaliana. Front. Plant Sci., 8, 2017, 39, 10.3389/fpls.2017.00039.
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821, 10.1126/science.1225829.
Haeussler, M., Concordet, J.-P., Genome Editing with CRISPR-Cas9: Can It Get Any Better?. J. Genet. Genomics 43 (2016), 239–250, 10.1016/j.jgg.2016.04.008.
Dang, Y., Jia, G., Choi, J., Ma, H., Anaya, E., Ye, C., Shankar, P., Wu, H., Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biol., 16, 2015, 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, S.H., LaFrance, B., Kaplan, M., Doudna, J.A., Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 527 (2015), 1–14, 10.1038/nature15544.
Xu, H., Xiao, T., Chen, C.-H., Li, W., Meyer, C.A., Wu, Q., Wu, D., Cong, L., Zhang, F., Liu, J.S., Brown, M., Liu, X.S., Sequence determinants of improved CRISPR sgRNA design. Genome Res. 25 (2015), 1147–1157, 10.1101/gr.191452.115.
Wong, N., Liu, W., Wang, X., WU-CRISPR: characteristics of functional guide RNAs for the CRISPR/Cas9 system. Genome Biol., 16, 2015, 218, 10.1186/s13059-015-0784-0.
Ding, Y., Li, H., Chen, L.-L., Xie, K., Recent advances in genome editing using CRISPR/Cas9. Front. Plant Sci., 7, 2016, 703, 10.3389/fpls.2016.00703.
Ren, X., Yang, Z., Xu, J., Sun, J., Mao, D., Hu, Y., Yang, S.-J., Qiao, H.-H., Wang, X., Hu, Q., Deng, P., Liu, L.-P., Ji, J.-Y., Li, J.B., Ni, J.-Q., Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila. Cell Rep. 9 (2014), 1151–1162, 10.1016/j.celrep.2014.09.044.
Farboud, B., Meyer, B.J., Dramatic enhancement of genome editing by CRISPR/Cas9 through improved guide RNA design. Genetics 199 (2015), 959–971, 10.1534/genetics.115.175166.
Collonnier, C., Epert, A., Mara, K., Maclot, F., Guyon-Debast, A., Charlot, F., White, C., Schaefer, D.G., Nogué, F., CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol. J., 2016, 1–10, 10.1111/pbi.12596.
Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, K., Liu, J., Xi, J.J., Qiu, J.-L., Gao, C., Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31 (2013), 686–688, 10.1038/nbt.2650.
Fauser, F., Schiml, S., Puchta, H., Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79 (2014), 348–359, 10.1111/tpj.12554.
He, X., Tan, C., Wang, F., Wang, Y., Zhou, R., Cui, D., You, W., Zhao, H., Ren, J., Feng, B., Knock-in of large reporter genes in human cells via CRISPR/Cas9-induced homology-dependent and independent DNA repair. Nucleic Acids Res., 44, 2016, 10.1093/nar/gkw064 e85–e85.
Komor, A.C., Kim, Y.B., Packer, M.S., Zuris, J.A., Liu, D.R., Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 61 (2016), 5985–5991, 10.1038/nature17946.
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, J., Sun, Y., Du, J., Zhao, Y., Xia, L., Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol. Plant., 2016, 526–529, 10.1016/j.molp.2016.12.001.
Lu, Y., Zhu, J., Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant., 2016, 523–525, 10.1016/j.molp.2016.11.013.
Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., Teramura, H., Yamamoto, T., Komatsu, H., Miura, K., Ezura, H., Nishida, K., Ariizumi, T., Kondo, A., Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol., 2017, 3–8, 10.1038/nbt.3833.
Komor, A.C., Badran, A.H., Liu, D.R., CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 168 (2016), 1–17, 10.1016/j.cell.2016.10.044.
Steinert, J., Schiml, S., Fauser, F., Puchta, H., Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. Plant J. 84 (2015), 1295–1305, 10.1111/tpj.13078.
Wright, A.V., Nuñez, J.K., Doudna, J.A., Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164 (2016), 29–44, 10.1016/j.cell.2015.12.035.
Shmakov, S., Abudayyeh, O.O., Makarova, K.S., Wolf, Y.I., Gootenberg, J.S., Semenova, E., Minakhin, L., Joung, J., Konermann, S., Severinov, K., Zhang, F., Koonin, E.V., Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell 60 (2015), 385–397, 10.1016/j.molcel.2015.10.008.
Fonfara, I., Richter, H., Bratovič, M., Le Rhun, A., Charpentier, E., The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532 (2016), 517–521, 10.1038/nature17945.
Hu, X., Wang, C., Liu, Q., Fu, Y., Wang, K., Targeted mutagenesis in rice using CRISPR-Cpf1 system. J. Genet. Genomics 44 (2016), 2016–2018, 10.1016/j.jgg.2016.12.001.
Kim, H., Kim, S.-T., Ryu, J., Kang, B.-C., Kim, J.-S., Kim, S.-G., CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat. Commun., 8, 2017, 14406, 10.1038/ncomms14406.
Tang, X., Lowder, L.G., Zhang, T., Malzahn, A.A., Zheng, X., Voytas, D.F., Zhong, Z., Chen, Y., Ren, Q., Li, Q., Kirkland, E.R., Zhang, Y., Qi, Y., A CRISPR–Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat. Plants., 3, 2017, 17018, 10.1038/nplants.2017.18.
Endo, A., Masafumi, M., Kaya, H., Toki, S., Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci. Rep., 6, 2016, 38169, 10.1038/srep38169.
Wang, L., Wang, L., Tan, Q., Fan, Q., Zhu, H., Hong, Z., Zhang, Z., Duanmu, D., Efficient inactivation of symbiotic nitrogen fixation related genes in Lotus japonicus Using CRISPR-Cas9. Front. Plant Sci., 7, 2016, 1333, 10.3389/fpls.2016.01333.
Yan, L., Wei, S., Wu, Y., Hu, R., Li, H., Yang, W., Xie, Q., High-efficiency genome editing in arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Mol. Plant 8 (2015), 1820–1823, 10.1016/j.molp.2015.10.004.
Mao, Y., Zhang, Z., Feng, Z., Wei, P., Zhang, H., Botella, J.R., Zhu, J.-K., Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol. J. 14 (2016), 519–532, 10.1111/pbi.12468.
Schiml, S., Puchta, H., Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas. Plant Methods, 12, 2016, 8, 10.1186/s13007-016-0103-0.
Chu, V.T., Weber, T., Wefers, B., Wurst, W., Sander, S., Rajewsky, K., Kühn, R., Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat. Biotechnol. 33 (2015), 543–548, 10.1038/nbt.3198.
Sakuma, T., Nakade, S., Sakane, Y., Suzuki, K.-I.T., Yamamoto, T., MMEJ-assisted gene knock-in using TALENs and CRISPR-Cas9 with the PITCh systems. Nat. Protoc. 11 (2015), 118–133, 10.1038/nprot.2015.140.
Sun, Y., Zhang, X., Wu, C., He, Y., Ma, Y., Hou, H., Guo, X., Du, W., Zhao, Y., Xia, L., Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant 9 (2016), 628–631, 10.1016/j.molp.2016.01.001.
Butler, N.M., Atkins, P.A., Voytas, D.F., Douches, D.S., Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas system. PLoS One, 10, 2015, e0144591, 10.1371/journal.pone.0144591.
Li, W., Teng, F., Li, T., Zhou, Q., Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat. Biotechnol. 31 (2013), 684–686, 10.1038/nbt.2652.
Richardson, C.D., Ray, G.J., DeWitt, M.A., Curie, G.L., Corn, J.E., Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol. 34 (2016), 339–344, 10.1038/nbt.3481.
Liang, X., Potter, J., Kumar, S., Ravinder, N., Chesnut, J.D., Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA. J. Biotechnol. 241 (2017), 136–146, 10.1016/j.jbiotec.2016.11.011.
Renaud, J.-B., Boix, C., Charpentier, M., De Cian, A., Cochennec, J., Duvernois-Berthet, E., Perrouault, L., Tesson, L., Edouard, J., Thinard, R., Cherifi, Y., Menoret, S., Fontanière, S., de Crozé, N., Fraichard, A., Sohm, F., Anegon, I., Concordet, J.-P., Giovannangeli, C., Improved genome editing efficiency and flexibility using modified oligonucleotides with TALEN and CRISPR-Cas9 nucleases. Cell Rep. 14 (2016), 2263–2272, 10.1016/j.celrep.2016.02.018.
Zhang, Y., Liang, Z., Zong, Y., Wang, Y., Liu, J., Chen, K., Qiu, J.-L., Gao, C., Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun., 7, 2016, 12617 doi:10.1038/ncomms12617.
Woo, J.W., Kim, J., Il Kwon, S., Corvalán, C., Cho, S.W., Kim, H., Kim, S.-G., Kim, S.-T., Choe, S., Kim, J., DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33 (2015), 1162–1164, 10.1038/nbt.3389.
Svitashev, S., Schwartz, C., Lenderts, B., Young, J.K., Mark Cigan, A., Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat. Commun., 7, 2016, 13274, 10.1038/ncomms13274.
Subburaj, S., Chung, S.J., Lee, C., Ryu, S.-M., Kim, D.H., Kim, J.-S., Bae, S., Lee, G.-J., Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep. 35 (2016), 1535–1544, 10.1007/s00299-016-1937-7.
Engler, C., Kandzia, R., Marillonnet, S., A one pot, one step, precision cloning method with high throughput capability. PLoS One, 3, 2008, 10.1371/journal.pone.0003647.
Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C.A., Smith, H.O., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6 (2009), 343–345, 10.1038/nmeth.1318.
Liang, G., Zhang, H., Lou, D., Yu, D., Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing. Sci. Rep., 6, 2016, 21451, 10.1038/srep21451.
Vad-Nielsen, J., Lin, L., Bolund, L., Nielsen, A.L., Luo, Y., Golden gate assembly of CRISPR gRNA expression array for simultaneously targeting multiple genes. Cell. Mol. Life Sci. 73 (2016), 4315–4325, 10.1007/s00018-016-2271-5.
Vazquez-Vilar, M., Bernabé-Orts, J.M., Fernandez-del-Carmen, A., Ziarsolo, P., Blanca, J., Granell, A., Orzaez, D., A modular toolbox for gRNA–Cas9 genome engineering in plants based on the GoldenBraid standard. Plant Methods, 12, 2016, 10, 10.1186/s13007-016-0101-2.
Lowder, L.G., Zhang, D., Baltes, N.J., Paul, J.W., Tang, X., Zheng, X., Voytas, D.F., Hsieh, T.-F., Zhang, Y., Qi, Y., A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. 169 (2015), 971–985, 10.1104/pp.15.00636.
Tang, X., Zheng, X., Qi, Y., Zhang, D., Cheng, Y., Tang, A., Voytas, D.F., Zhang, Y., A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Mol. Plant 9 (2016), 1088–1091, 10.1016/j.molp.2016.05.001.
Xie, K., Minkenberg, B., Yang, Y., Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 3570–3575, 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, L., Perli, S.D., Fridkin, A., Perez-Pinera, P., Lu, T.K., Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol. Cell 54 (2014), 698–710, 10.1016/j.molcel.2014.04.022.
Osakabe, Y., Watanabe, T., Sugano, S.S., Ueta, R., Ishihara, R., Shinozaki, K., Osakabe, K., Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci. Rep., 6, 2016, 26685, 10.1038/srep26685.
Baltes, N.J., Hummel, A.W., Konecna, E., Cegan, R., Bruns, A.N., Bisaro, D.M., Voytas, D.F., Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat. Plants, 1, 2015, 15145, 10.1038/nplants.2015.145.
Yin, K., Han, T., Liu, G., Chen, T., Wang, Y., Yu, A.Y.L., Liu, Y., A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci. Rep., 5, 2015, 14926, 10.1038/srep14926.
Larsen, J.S., Curtis, W.R., RNA viral vectors for improved Agrobacterium -mediated transient expression of heterologous proteins in Nicotiana benthamiana cell suspensions and hairy roots. BMC Biotechnol. 12 (2012), 1–11.
Alagoz, Y., Gurkok, T., Zhang, B., Unver, T., 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., 2016, 1–9, 10.1038/srep30910.
Gil-Humanes, J., Wang, Y., Liang, Z., Shan, Q., Ozuna, C.V., Sánchez-León, S., Baltes, N.J., Starker, C., Barro, F., Gao, C., Voytas, D.F., High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J. 89 (2017), 1251–1262, 10.1111/tpj.13446.
Malnoy, M., Viola, R., Jung, M., Koo, O., Kim, S., Kim, J., Velasco, R., Kanchiswamy, C.N., DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front. Plant Sci. 7 (2016), 1–9, 10.3389/fpls.2016.01904.
Burstein, D., Harrington, L.B., Strutt, S.C., Probst, A.J., Anantharaman, K., Thomas, B.C., Doudna, J.A., Banfield, J.F., New CRISPR-Cas systems from uncultivated microbes. Nature, 2016, 1–20, 10.1038/nature21059.
Pierce, A.J., Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15 (2001), 3237–3242, 10.1101/gad.946401.
Delacôte, F., Han, M., Stamato, T.D., Jasin, M., Lopez, B.S., An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res. 30 (2002), 3454–3463, 10.1093/nar/gkf452.
Qi, Y., Zhang, Y., Zhang, F., Baller, J.A., Cleland, S.C., Ryu, Y., Starker, C.G., Voytas, D.F., Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways. Genome Res. 23 (2013), 547–554, 10.1101/gr.145557.112.
Gutschner, T., Haemmerle, M., Genovese, G., Draetta, G.F., Chin, L., Post-translational regulation of Cas9 during G1 enhances homology-directed repair. Cell Rep. 14 (2016), 1555–1566, 10.1016/j.celrep.2016.01.019.
Howden, S.E., McColl, B., Glaser, A., Vadolas, J., Petrou, S., Little, M.H., Elefanty, A.G., Stanley, E.G., A Cas9 variant for efficient generation of indel-free knockin or gene-corrected human pluripotent stem cells. Stem Cell Rep. 7 (2016), 508–517, 10.1016/j.stemcr.2016.07.001.
Saintigny, Y., Delacôte, F., Boucher, D., Averbeck, D., Lopez, B.S., XRCC4 in G1 suppresses homologous recombination in S/G2, in G1 checkpoint-defective cells. Oncogene 26 (2007), 2769–2780, 10.1038/sj.onc.1210075.
Saleh-Gohari, N., Helleday, T., Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res. 32 (2004), 3683–3688, 10.1093/nar/gkh703.
Maruyama, T., Dougan, S.K., Truttmann, M.C., Bilate, A.M., Ingram, J.R., Ploegh, H.L., Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33 (2015), 538–542, 10.1038/nbt.3190.
Yu, C., Liu, Y., Ma, T., Liu, K., Xu, S., Zhang, Y., Liu, H., La Russa, M., Xie, M., Ding, S., Qi, L.S., Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16 (2015), 142–147, 10.1016/j.stem.2015.01.003.
Hanin, M., Paszkowski, J., Plant genome modification by homologous recombination. Curr. Opin. Plant Biol. 6 (2003), 157–162 http://www.ncbi.nlm.nih.gov/pubmed/12667873.
Schaefer, D.G., A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu. Rev. Plant Biol. 53 (2002), 477–501, 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, B., Schaefer, D.G., Charlot, F., Nogué, F., MSH2 is essential for the preservation of genome integrity and prevents homeologous recombination in the moss Physcomitrella patens. Nucleic Acids Res. 34 (2006), 232–242, 10.1093/nar/gkj423.
Kamisugi, Y., Schaefer, D.G., Kozak, J., Charlot, F., Vrielynck, N., Holá, M., Angelis, K.J., Cuming, A.C., Nogué, F., MRE11 and RAD50, but not NBS1, are essential for gene targeting in the moss Physcomitrella patens. Nucleic Acids Res. 40 (2012), 3496–3510, 10.1093/nar/gkr1272.
Schaefer, D.G., Delacote, F., Charlot, F., Vrielynck, N., Guyon-Debast, A., Le Guin, S., Neuhaus, J.M., Doutriaux, M.P., Nogué, F., RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens. DNA Repair (Amst) 9 (2010), 526–533, 10.1016/j.dnarep.2010.02.001.
Trouiller, B., Charlot, F., Choinard, S., Schaefer, D.G., Nogué, F., Comparison of gene targeting efficiencies in two mosses suggests that it is a conserved feature of Bryophyte transformation. Biotechnol. Lett. 29 (2007), 1591–1598, 10.1007/s10529-007-9423-5.
Puchta, H., Fauser, F., Gene targeting in plants: 25 years later. Int. J. Dev. Biol. 57 (2013), 629–637, 10.1387/ijdb.130194hp.
Kamisugi, Y., Schlink, K., Rensing, S.A., Schween, G., von Stackelberg, M., Cuming, A.C., Reski, R., Cove, D.J., The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res. 34 (2006), 6205–6214, 10.1093/nar/gkl832.
Schaefer, D.G., Zrÿd, J.P., Efficient gene targeting in the moss Physcomitrella patens. Plant J. 11 (1997), 1195–1206 http://www.ncbi.nlm.nih.gov/pubmed/9225463.
Charlot, F., Chelysheva, L., Kamisugi, Y., Vrielynck, N., Guyon, A., Epert, A., Le Guin, S., Schaefer, D.G., Cuming, A.C., Grelon, M., Nogué, F., RAD51B plays an essential role during somatic and meiotic recombination in Physcomitrella. Nucleic Acids Res. 42 (2014), 11965–11978, 10.1093/nar/gku890.
Waltz, E., CRISPR-edited crops free to enter market, skip regulation. Nat. Biotechnol., 34, 2016, 10.1038/nbt0616-582 582–582.
Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., RNA-guided human genome engineering via Cas9. Science 339 (2013), 823–826, 10.1126/science.1232033.
Ashton, N.W., Cove, D.J., The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens. Mol. Gen. Genet. MGG. 154 (1977), 87–95, 10.1007/BF00265581.
