Plant genome editing using engineered nucleases and success of CRISPR/Cas9 system

Moon Sajid, Zohaib Hassan, Ghulam Hussain Sehrai, Muhammad Adeel Rana, Holger Puchta, Abdul Qayyum Rao

Abstract


Development of new plant breeding techniques have facilitated easy manipulation of plants at genetic level. Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/CRISPR associated protein9 (Cas9) system is a valuable addition in programmable nucleases. The CRISPR/Cas9 system uses an RNA component to recognize a target DNA sequences and it has shown promising results with respect to simultaneous editing of multigenic plant traits. In this review, components of CRISPR/Cas9, their construction and its methods of delivery to plant cells are analyzed. Variation in nucleotide sequence of the protospacer adjacent motif, codon optimization and progress in web-based bioinformatic tools, will make CRISPR/Cas9 systems more efficient for plants. Development and optimization of protocols to efficiently target all plant species is still under development. Along with this, methods to inspect induced mutation and efficiency of the system have also been reviewed. Auxiliary improvements and understanding are still required to expand the CRISPR/Cas9 systems to target complex genome architectures and epigenetic elements.


Full Text:

PDF

References


Kumar S, Barone P, Smith M. Gene targeting and transgene stacking using intra genomic homologous recombination in plants. Plant Methods, (2016); 12(1): 1.

Puspito AN, Rao AQ, Hafeez MN, Iqbal MS, Bajwa KS, et al. Transformation and Evaluation of Cry1Ac+Cry2A and GTGene in Gossypium hirsutum L. Frontiers in Plant Science, (2015); 6(943): 1-13.

Bajwa KS, Shahid AA, Rao AQ, Kiani MS, Ashraf MA, et al. Expression of Calotropis procera expansin gene CpEXPA3 enhances cotton fibre strength. Australian Journal of Crop Science, (2013); 7(2): 206-212.

Muzaffar A, Kiani S, Khan MAU, Rao AQ, Ali A, et al. Chloroplast localization of Cry1Ac and Cry2A protein-an alternative way of insect control in cotton. Biological research, (2015); 48(1): 14.

Yaqoob A, Shahid AA, Samiullah TR, Rao AQ, Khan MAU, et al. Risk assessment of Bt crops on the non‐target plant‐associated insects and soil organisms. Journal of the Science of Food and Agriculture, (2016); 96(8): 2613-2619.

Yasmeen A, Kiani S, Butt A, Rao AQ, Akram F, et al. Amplicon-Based RNA Interference Targeting V2 Gene of Cotton Leaf Curl Kokhran Virus-Burewala Strain Can Provide Resistance in Transgenic Cotton Plants. Molecular biotechnology, (2016); 58(12): 807-820.

Rao AQ, Bakhsh A, Nasir IA, Riazuddin S, Husnain T. Phytochrome B mRNA expression enhances biomass yield and physiology of cotton plants. African Journal of Biotechnology, (2011); 10(10): 1818-1826.

Rao AQ, Irfan M, Saleem Z, Nasir IA, Riazuddin S, et al. Overexpression of the phytochrome B gene from Arabidopsis thaliana increases plant growth and yield of cotton (Gossypium hirsutum). Journal of Zhejiang University-Science B, (2011); 12(4): 326-334.

Puchta H. The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. Journal of Experimental Botany, (2005); 56(409): 1-14.

Salomon S, Puchta H. Capture of genomic and T‐DNA sequences during double‐strand break repair in somatic plant cells. The EMBO journal, (1998); 17(20): 6086-6095.

Puchta H, Dujon B, Hohn B. Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proceedings of the National Academy of Sciences, (1996); 93(10): 5055-5060.

Steinert J, Schiml S, Puchta H. Homology-based double-strand break-induced genome engineering in plants. Plant Cell Reports, (2016); 1-10.

Puchta H, Fauser F. Gene targeting in plants: 25 years later. International Journal of Developmental Biology, (2013); 57(6-7-8): 629-637.

Puchta H. Using CRISPR/Cas in three dimensions: towards synthetic plant genomes, transcriptomes and epigenomes. The Plant Journal, (2016); 87(1): 5-15.

Ma X, Zhu Q, Chen Y, Liu Y-G. CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Molecular Plant, (2016); 9(7): 961-974.

Antunes MS, Smith JJ, Jantz D, Medford JI. Targeted DNA excision in Arabidopsis by a re-engineered homing endonuclease. BMC Biotechnology, (2012); 12(86): 1-12.

Miller JC, Holmes MC, Wang J, Guschin DY, Lee Y-L, et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotechnology, (2007); 25(7): 778-785.

Xie K, Yang Y. RNA-Guided Genome Editing in Plants Using a CRISPR–Cas System. Molecular Plant, (2013); 6(6): 1975-1983.

Smith J, Bibikova M, Whitby FG, Reddy A, Chandrasegaran S, et al. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Research, (2000); 28(17): 3361-3369.

Smith J, Grizot S, Arnould S, Duclert A, Epinat JC, et al. A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Research, (2006); 34(22): e149-e149.

Miller JC, Tan S, Qiao G, Barlow KA, Wang J, et al. A TALE nuclease architecture for efficient genome editing. Nature Biotechnology, (2011); 29(2): 143-148.

Li J-F, Norville JE, Aach J, McCormack M, Zhang D, et al. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, (2013); 31(8): 688-691.

Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, et al. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science, (2012); 337(6096): 816-821.

Jiang F, Doudna JA. CRISPR-Cas9 Structures and Mechanisms. Annual Review of Biophysics, (2017); 46(1): 509-529.

Demirci Y, Zhang B, Unver T. CRISPR/Cas9: an RNA‐guided highly precise synthetic tool for plant genome editing. Journal of Cellular Physiology, (2017); 9999: 1-16.

Khatodia S, Bhatotia K, Tuteja N. Development of CRISPR/Cas9 mediated virus resistance in agriculturally important crops. Bioengineered, (2017); 8(3): 274-279.

Gerasimova S, Khlestkina E, Kochetov A, Shumny V. Genome editing system CRISPR/CAS9 and peculiarities of its application in monocots. Russian Journal of Plant Physiology, (2017); 64(2): 141-155.

Leonova I. Molecular markers: Implementation in crop plant breeding for identification, introgression and gene pyramiding. Russian Journal of Genetics: Applied Research, (2013); 3(6): 464-473.

Rao AQ, Irfan M, Saleem Z, Nasir IA, Riazuddin S, et al. Overexpression of the phytochrome B gene from Arabidopsis thaliana increases plant growth and yield of cotton (Gossypium hirsutum). Journal of Zhejiang University SCIENCE B, (2011); 12(4): 326-334.

Wright AV, Nuñez JK, Doudna JA. Biology and Applications of CRISPR Systems: Harnessing Nature’s Toolbox for Genome Engineering. Cell, (2016); 164(1): 29-44.

Weeks DP, Spalding MH, Yang B. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnology Journal, (2016); 14(2): 483-495.

Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V. Editing plant genomes with CRISPR/Cas9. Current Opinion in Biotechnology, (2015); 3276-84.

Xie K, Zhang J, Yang Y. Genome-wide prediction of highly specific guide RNA spacers for CRISPR–Cas9-mediated genome editing in model plants and major crops. Molecular Plant, (2014); 7(5): 923-926.

Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, (2014); 507(7490): 62-67.

Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, et al. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, (2014); 156(5): 935-949.

Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant methods, (2013); 9(39): 1-12.

Xu R-F, Li H, Qin R-Y, Li J, Qiu C-H, et al. Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Scientific Reports, (2015); 511491.

Gao Y, Zhao Y. Self‐processing of ribozyme‐flanked RNAs into guide RNAs in vitro and in vivo for CRISPR‐mediated genome editing. Journal of Integrative Plant Biology, (2014); 56(4): 343-349.

Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature, (2015); 520(7546): 186-191.

Wright AV, Sternberg SH, Taylor DW, Staahl BT, Bardales JA, et al. Rational design of a split-Cas9 enzyme complex. Proceedings of the National Academy of Sciences, (2015); 112(10): 2984-2989.

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular Plant, (2015); 8(8): 1274-1284.

Jiang W, Zhou H, Bi H, Fromm M, Yang B, et al. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research, (2013); 41(20): e188.

Shan Q, Wang Y, Li J, Zhang Y, Chen K, et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology, (2013); 31(8): 686-688.

Yoo S-D, Cho Y-H, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature protocols, (2007); 2(7): 1565-1572.

Van der Hoorn RA, Laurent F, Roth R, De Wit PJ. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr 9/Cf-9-induced and Avr 4/Cf-4-induced necrosis. Molecular Plant-Microbe Interactions, (2000); 13(4): 439-446.

Kumar V, Jain M. The CRISPR–Cas system for plant genome editing: advances and opportunities. Journal of Experimental Botany, (2015); 66(1): 47-57.

Rivera AL, Gómez-Lim M, Fernández F, Loske AM. Physical methods for genetic plant transformation. Physics of Life Reviews, (2012); 9(3): 308-345.

Vazquez-Vilar M, Bernabé-Orts JM, Fernandez-del-Carmen A, Ziarsolo P, Blanca J, et al. A modular toolbox for gRNA–Cas9 genome engineering in plants based on the GoldenBraid standard. Plant Methods, (2016); 12(1): 10.

Xie K, Minkenberg B, Yang Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proceedings of the National Academy of Sciences, (2015); 112(11): 3570-3575.

Zhou H, Liu B, Weeks DP, Spalding MH, Yang B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Research, (2014); 42(17): 10903-14.

Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, et al. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiology, (2015); 169(2): 971-985.

Zhu J, Song N, Sun S, Yang W, Zhao H, et al. Efficiency and inheritance of targeted mutagenesis in maize using CRISPR-Cas9. Journal of Genetics and Genomics, (2016); 43(1): 25-36.

Dahlem TJ, Hoshijima K, Jurynec MJ, Gunther D, Starker CG, et al. Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genetic, (2012); 8(8): e1002861.

Fauser F, Schiml S, Puchta H. Both CRISPR/Cas‐based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. The Plant Journal, (2014); 79(2): 348-359.

Feng Z, Mao Y, Xu N, Zhang B, Wei P, et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences, (2014); 111(12): 4632-4637.

Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotechnology, (2013); 31(9): 822-826.

Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nature Biotechnology, (2013); 31(9): 827-832.

Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nature Biotechnology, (2013); 31(9): 833-838.

Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA, et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nature Biotechnology, (2013); 31(9): 839-843.

Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nature Biotechnology, (2013); 31(3): 233-239.

Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, et al. Rationally engineered Cas9 nucleases with improved specificity. Science, (2016); 351(6268): 84-88.

Dang Y, Jia G, Choi J, Ma H, Anaya E, et al. Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biology, (2015); 16(1): 1-10.

Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, (2013); 154(6): 1380-1389.

Shen B, Zhang W, Zhang J, Zhou J, Wang J, et al. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nature Methods, (2014); 11(4): 399-402.

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. The Plant Journal, (2014); 80(6): 1139-1150.

Mikami M, Toki S, Endo M. Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant and Cell Physiology, (2016); pcw049.

Schiml S, Fauser F, Puchta H. Repair of adjacent single-strand breaks is often accompanied by the formation of tandem sequence duplications in plant genomes. Proceedings of the National Academy of Sciences, (2016); 201603823.

Wang Y, Liu X, Ren C, Zhong G-Y, Yang L, et al. Identification of genomic sites for CRISPR/Cas9-based genome editing in the Vitis vinifera genome. BMC Plant Biology, (2016); 16(1): 1-7.

Gantz VM, Bier E. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science, (2015); 348(6233): 442-444.

Ledford H. CRISPR, the disruptor. Nature, (2015); 522(7554): 20-24.

Duke SO. Perspectives on transgenic, herbicide‐resistant crops in the United States almost 20 years after introduction. Pest Management Science, (2015); 71(5): 652-657.

Plagens A, Richter H, Charpentier E, Randau L. DNA and RNA interference mechanisms by CRISPR-Cas surveillance complexes. FEMS Microbiology Reviews, (2015); 39(3): 442-463.

Lawrenson T, Shorinola O, Stacey N, Li C, Østergaard L, et al. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biology, (2015); 16(1): 1-13.

Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature, (2015); 523(7561): 481-485.

Kleinstiver BP, Prew MS, Tsai SQ, Nguyen NT, Topkar VV, et al. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nature Biotechnology, (2015).

Hu X, Wang C, Fu Y, Liu Q, Jiao X, et al. Expanding the Range of CRISPR/Cas9 Genome Editing in Rice. Molecular plant, (2016); 9(6): 943-945.

Endo A, Masafumi M, Kaya H, Toki S. Efficient targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Scientific Reports, (2016); 6: 38169.

Steinert J, Schiml S, Fauser F, Puchta H. Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. The Plant Journal, (2015); 84(6): 1295-1305.




DOI: http://dx.doi.org/10.62940/als.v4i4.477

Refbacks

  • There are currently no refbacks.