Towards CRISPR/CAS crops – Bringing together genomics and genome editing

New Phytologist

Volumn 216, Issue 3, 2017, Pages 682-698

  Scheben, Armin ^a   Wolter, Felix ^b   Batley, Jacqueline ^a   Puchta, Holger ^b   Edwards, David ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Breeding; Cas; CRISPR; Crops; Gene targeting (GT); Genome editing; Targeted mutagenesis

Indexed keywords

CLIMATE CHANGE; CROP IMPROVEMENT; CROP PLANT; CROP YIELD; GENE EXPRESSION; GENOME; GENOMICS; HIGH YIELDING VARIETY; PROTEIN; RECOMBINATION; TOLERANCE;

CRISPR CAS SYSTEM; CROP; GENE EDITING; GENETIC RECOMBINATION; GENETICS; PLANT BREEDING; PLANT GENOME; PROCEDURES; TRANSGENIC PLANT;

CRISPR-CAS SYSTEMS; CROPS, AGRICULTURAL; GENE EDITING; GENOME, PLANT; PLANT BREEDING; PLANTS, GENETICALLY MODIFIED; RECOMBINATION, GENETIC;

EID: 85026510003     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14702     Document Type: Review

References (152)

1. Acquaah G. 2012. Principles of plant genetics and breeding. Chichester, UK: Wiley-Blackwell.
2. Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM. 2015. CRISPR/ Cas9-mediated viral interference in plants. Genome Biology 16: 238.
3. Altpeter F, Springer NM, Bartley LE, Blechl AE, Brutnell TP, Citovsky V, Conrad LJ, Gelvin SB, Jackson DP, Kausch AP et al. 2016. Advancing crop transformation in the era of genome editing. Plant Cell 28: 1510–1520.
4. Andolfo G, Iovieno P, Frusciante L, Ercolano MR. 2016. Genome-editing technologies for enhancing plant disease resistance. Frontiers in Plant Science 7: 1813.
5. Andorf CM, Cannon EK, Portwood JL, Gardiner JM, Harper LC, Schaeffer ML, Braun BL, Campbell DA, Vinnakota AG, Sribalusu VV et al. 2016. MaizeGDB update: new tools, data and interface for the maize model organism database. Nucleic Acids Research 44: D1195–D1201.
6. Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF. 2014. DNA replicons for plant genome engineering. Plant Cell 26: 151–163.
7. Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN, Bisaro DM, Voytas DF. 2015. Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nature Plants 1: 15145.
8. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V. 2015. Editing plant genomes with CRISPR/Cas9. Current Opinion in Biotechnology 32: 76–84.
9. Blomstedt CK, Gleadow RM, O’Donnell N, Naur P, Jensen K, Laursen T, Olsen CE, Stuart P, Hamill JD, Moller BL et al. 2012. A combined biochemical screen and TILLING approach identifies mutations in Sorghum bicolor L. Moench resulting in acyanogenic forage production. Plant Biotechnology Journal 10:54–66.
10. Bortesi L, Fischer R. 2015. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnology Advances 33:41–52.
11. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nature Methods 10: 1213–1218.
12. Canadian Food Inspection Agency. 2016. Plants with novel traits. [WWW document] URL http://www.inspection.gc.ca/plants/plants-with-novel-traits/eng/1300137887237/1300137939635 [accessed 8 May 2017].
13. Carpenter JE. 2010. Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nature Biotechnology 28: 319–321.
14. Cermak T, Baltes NJ, Cegan R, Zhang Y, Voytas DF. 2015. High-frequency, precise modification of the tomato genome. Genome Biology 16: 232.
15. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A. 2016. Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Molecular Plant Pathology 17: 1140–1153.
16. Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A et al. 2016. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnology Journal 14: 169–176.
17. Collard BC, Mackill DJ. 2008. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society B 363: 557–572.
18. Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dahlborg EJ, Goodwin MJ, Coffman AP et al. 2011. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiology 156:466–473.
19. Dang Y, Jia G, Choi J, Ma H, Anaya E, Ye C, Shankar P, Wu H. 2015. Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biology 16: 280.
20. Daniell H. 2002. Molecular strategies for gene containment in transgenic crops. Nature Biotechnology 20: 581–586.
21. Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA. 2012. PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Research 40: D1194–D1201.
22. Demorest ZL, Coffman A, Baltes NJ, Stoddard TJ, Clasen BM, Luo S, Retterath A, Yabandith A, Gamo ME, Bissen J et al. 2016. Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil. BMC Plant Biology 16: 225.
23. Desta ZA, Ortiz R. 2014. Genomic selection: genome-wide prediction in plant improvement. Trends in Plant Science 19: 592–601.
24. Doebley JF, Gaut BS, Smith BD. 2006. The molecular genetics of crop domestication. Cell 127: 1309–1321.
25. Edwards D. 2016. The impact of genomics technology on adapting plants to climate change. In: Edwards D, Batley J, eds. Plant genomics and climate change. New York, NY, USA: Springer, 173–178.
26. Eeckhaut T, Lakshmanan PS, Deryckere D, Van Bockstaele E, Van Huylenbroeck J. 2013. Progress in plant protoplast research. Planta 238: 991–1003.
27. Eid A, Ali Z, Mahfouz MM. 2016. High efficiency of targeted mutagenesis in Arabidopsis via meiotic promoter-driven expression of Cas9 endonuclease. Plant Cell Reports 35: 1555–1558.
28. Fauser F, Roth N, Pacher M, Ilg G, Sanchez-Fernandez R, Biesgen C, Puchta H. 2012. In planta gene targeting. Proceedings of the National Academy of Sciences, USA 109: 7535–7540.
29. 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 Journal 79: 348–359.
30. Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang D-L, Wang Z, Zhang Z, Zheng R, Yang L et al. 2014. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences, USA 111: 4632–4637.
31. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotechnology 31: 822–826.
32. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology 32:279–284.
33. Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proceedings of the National Academy of Sciences, USA 109: E2579–E2586.
34. Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV, Sanchez-Leon S, Baltes NJ, Starker C, Barro F, Gao C et al. 2017. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant Journal 89: 1251–1262.
35. Gilbert LA, Larson MH, Morsut L, Liu ZR, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154: 442–451.
36. Golicz AA, Batley J, Edwards D. 2016a. Towards plant pangenomics. Plant Biotechnology Journal 14: 1099–1105.
37. Golicz AA, Bayer PE, Barker GC, Edger PP, Kim H, Martinez PA, Chan CK, Severn-Ellis A, McCombie WR, Parkin IA et al. 2016b. The pangenome of an agronomically important crop plant Brassica oleracea. Nature Communications 7:13390.
38. Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M, Williamson RJ, Forczek E, Joly-Lopez Z, Steffen JG, Hazzouri KM et al. 2013. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nature Genetics 45: 891–898.
39. Heigwer F, Kerr G, Boutros M. 2014. E-CRISP: fast CRISPR target site identification. Nature Methods 11: 122–124.
40. Hilton IB, D’Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA. 2015. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nature Biotechnology 33: 510–517.
41. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li YQ, Fine EJ, Wu XB, Shalem O et al. 2013. DNA targeting specificity of RNA-guided Cas9 nucleases. Nature Biotechnology 31: 827–832.
42. Hu HH, Xiong LZ. 2014. Genetic engineering and breeding of drought-resistant crops. Annual Review of Plant Biology 65: 715–741.
43. 4 photosynthesis in the grasses. Journal of Experimental Botany 68: 127–135.
44. Iaffaldano B, Zhang YX, Cornish K. 2016. CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection. Industrial Crops and Products 89: 356–362.
45. IPCC, Barros VR, Field CB, Dokke DJ, Mastrandrea MD, Mach KJ, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC et al., eds. 2014. Climate Change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of Working Group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
46. Ishida Y, Hiei Y, Komari T. 2007. Agrobacterium-mediated transformation of maize. Nature Protocols 2: 1614–1621.
47. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Toki S. 2015. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochemical and Biophysical Research Communications 467:76–82.
48. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA. 2015. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnology 15: 16.
49. Ji X, Zhang HW, Zhang Y, Wang YP, Gao CX. 2015. Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nature Plants 1: 15 144.
50. Jiang WZ, Zhou HB, Bi HH, Fromm M, Yang B, Weeks DP. 2013. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Research 41: e188.
51. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–821.
52. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng ZL, Joung JK. 2016. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529: 490–495.
53. Koike-Yusa H, Li Y, Tan EP, Velasco-Herrera Mdel C, Yusa K. 2014. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nature Biotechnology 32: 267–273.
54. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533: 420–424.
55. Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H et al. 2015. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517: 583–588.
56. Lambert B, Denolf P, Engelen S, Golds T, Haesendonckx B, Ruiter R, Robbens S, Bots M, Laga B. 2015. Omics-directed reverse genetics enables the creation of new productivity traits for the vegetable oil crop canola. Procedia Environmental Sciences 29:77–78.
57. Lawrenson T, Shorinola O, Stacey N, Li C, Ostergaard L, Patron N, Uauy C, Harwood W. 2015. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biology 16: 258.
58. Lee HJ, Kweon J, Kim E, Kim S, Kim JS. 2012. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Research 22: 539–548.
59. Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H. 2016b. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Frontiers in Plant Science 7: 377.
60. Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C. 2016a. Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nature Plants 2: 16139.
61. Li J-F, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J. 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology 31: 688–691.
62. Li Z, Liu Z-B, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM. 2015. Cas9-guide RNA directed genome editing in soybean. Plant Physiology 169: 960–970.
63. Liang Z, Chen KL, Li TD, Zhang Y, Wang YP, Zhao Q, Liu JX, Zhang HW, Liu CM, Ran YD et al. 2017. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nature Communications 8: 14261.
64. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326: 289–293.
65. Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, Voytas DF, Hsieh T-F, Zhang Y, Qi Y. 2015. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiology 169: 971–985.
66. Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho MJ, Scelonge C, Lenderts B, Chamberlin M, Cushatt J et al. 2016. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28: 1998–2015.
67. Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y et al. 2015. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular Plant 8: 1274–1284.
68. Massawe F, Mayes S, Cheng A. 2016. Crop diversity: an unexploited treasure trove for food security. Trends in Plant Science 21: 365–368.
69. Matson PA, Parton WJ, Power AG, Swift MJ. 1997. Agricultural intensification and ecosystem properties. Science 277: 504–509.
70. McCallum CM, Comai L, Greene EA, Henikoff S. 2000. Targeted screening for induced mutations. Nature Biotechnology 18: 455–457.
71. Michael TP, VanBuren R. 2015. Progress, challenges and the future of crop genomes. Current Opinion in Plant Biology 24:71–81.
72. Mickelbart MV, Hasegawa PM, Bailey-Serres J. 2015. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nature Reviews Genetics 16: 237–251.
73. Mikami M, Toki S, Endo M. 2016. Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant and Cell Physiology 57: 1058–1068.
74. Mikkelsen MD, Olsen CE, Halkier BA. 2010. Production of the cancer-preventive glucoraphanin in tobacco. Molecular Plant 3: 751–759.
75. Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. 2014. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Research 42: W401–W407.
76. Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S. 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nature Biotechnology 31: 691–693.
77. Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S. 2017. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Scientific Reports 7: 482.
78. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, Ishitani R, Zhang F, Nureki O. 2014. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156: 935–949.
79. Nobuta K, Venu RC, Lu C, Belo A, Vemaraju K, Kulkarni K, Wang WZ, Pillay M, Green PJ, Wang GL et al. 2007. An expression atlas of rice mRNAs and small RNAs. Nature Biotechnology 25: 473–477.
80. Ordon J, Gantner J, Kemna J, Schwalgun L, Reschke M, Streubel J,Boch J,Stuttmann J. 2016. Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit. Plant Journal 89: 155–168.
81. Osterberg JT, Xiang W, Olsen LI, Edenbrandt AK, Vedel SE, Christiansen A, Landes X, Andersen MM, Pagh P, Sandoe P et al. 2017. Accelerating the domestication of new crops: feasibility and approaches. Trends in Plant Science 22: 373–384.
82. Pacher M, Schmidt-Puchta W, Puchta H. 2007. Two unlinked double-strand breaks can induce reciprocal exchanges in plant genomes via homologous recombination and nonhomologous end joining. Genetics 175:21–29.
83. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068–1071.
84. Pattanayak V, Lin S, Guilinger JP, Ma EB, Doudna JA, Liu DR. 2013. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nature Biotechnology 31: 839–843.
85. Peciña A, Smith KN, Méezard C, Murakami H, Ohta K, Nicolas A. 2002. Targeted stimulation of meiotic recombination. Cell 111: 173–184.
86. Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X. 2017. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnology Journal 10: 1011–1013.
87. Peterson BA, Haak DC, Nishimura MT, Teixeira PJPL, James SR, Dangl JL, Nimchuk ZL. 2016. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLoS ONE 11: e0162169.
88. Puchta H. 2005. The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. Journal of Experimental Botany 56:1–14.
89. Puchta H. 2016. Using CRISPR/Cas in three dimensions: towards synthetic plant genomes, transcriptomes and epigenomes. Plant Journal 87:5–15.
90. Puchta H. 2017. Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Current Opinion in Plant Biology 36:1–8.
91. Qi W, Zhu T, Tian Z, Li C, Zhang W, Song R. 2016. High-efficiency CRISPR/ Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize. BMC Biotechnology 16: 58.
92. Radivojac P, Clark WT, Oron TR, Schnoes AM, Wittkop T, Sokolov A, Graim K, Funk C, Verspoor K, Ben-Hur A et al. 2013. A large-scale evaluation of computational protein function prediction. Nature Methods 10: 221–227.
93. Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380–1389.
94. Ranganathan V, Wahlin K, Maruotti J, Zack DJ. 2014. Expansion of the CRISPR-Cas9 genome targeting space through the use of H1 promoter-expressed guide RNAs. Nature Communications 5: 4516.
95. Ray DK, Mueller ND, West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8: e66428.
96. Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA. 2012. Recent patterns of crop yield growth and stagnation. Nature Communications 3: 1293.
97. Rousseau C, Gonnet M, Le Romancer M, Nicolas J. 2009. CRISPI: a CRISPR interactive database. Bioinformatics 25: 3317–3318.
98. Ruprecht C, Vaid N, Proost S, Persson S, Mutwil M. 2017. Beyond genomics: studying evolution with gene coexpression networks. Trends in Plant Science 22: 298–307.
99. Sadhu MJ, Bloom JS, Day L, Kruglyak L. 2016. CRISPR-directed mitotic recombination enables genetic mapping without crosses. Science 352: 1113–1116.
100. Sanjana NE, Wright J, Zheng K, Shalem O, Fontanillas P, Joung J, Cheng C, Regev A, Zhang F. 2016. High-resolution interrogation of functional elements in the noncoding genome. Science 353: 1545–1549.
101. Schaeffer SM, Nakata PA. 2015. CRISPR/Cas9-mediated genome editing and gene replacement in plants: transitioning from lab to field. Plant Science 240: 130–142.
102. Scheben A, Edwards D. 2017. Genome editors take on crops. Science 355: 1122–1123.
103. 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 Journal 80: 1139–1150.
104. 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 genomes. Proceedings of the National Academy of Sciences, USA 113: 7266–7271.
105. Schinkel H, Schillberg S. 2016. Genome editing: intellectual property and product development in plant biotechnology. Plant Cell Reports 35: 1487–1491.
106. Sedbrook JC, Phippen WB, Marks MD. 2014. New approaches to facilitate rapid domestication of a wild plant to an oilseed crop: example pennycress (Thlaspi arvense L.). Plant Science 227: 122–132.
107. Sekhon RS, Lin HN, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM. 2011. Genome-wide atlas of transcription during maize development. Plant Journal 66: 553–563.
108. Shan QW, Wang YP, Li J, Zhang Y, Chen KL, Liang Z, Zhang K, Liu JX, Xi JJ, Qiu JL et al. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nature Biotechnology 31: 686–688.
109. Shapter FM, Cross M, Ablett G, Malory S, Chivers IH, King GJ, Henry RJ. 2013. High-Throughput sequencing and mutagenesis to accelerate the domestication of Microlaena stipoides as a new food crop. PLoS ONE 8: e82641.
110. Sharwood RE. 2017. Engineering chloroplasts to improve Rubisco catalysis: prospects for translating improvements into food and fiber crops. New Phytologist 213: 494–510.
111. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE. 2016. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnology Journal 15: 207–216.
112. Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N, Yan W, Abudayyeh OO, Gootenberg JS, Makarova KS, Wolf YI et al. 2017. Diversity and evolution of class 2 CRISPR-Cas systems. Nature Reviews Microbiology 15: 169–182.
113. Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D. 2005. A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nature Biotechnology 23:75–81.
114. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. 2016. Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88.
115. Solomon MJ, Larsen PL, Varshavsky A. 1988. Mapping protein-DNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene. Cell 53: 937–947.
116. Soyk S, Muller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jimenez-Gomez JM, Lippman ZB. 2017. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nature Genetics 49: 162–168.
117. Steinert J, Schiml S, Fauser F, Puchta H. 2015. Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. Plant Journal 84: 1295–1305.
118. Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L. 2016. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Molecular Plant 9: 628–631.
119. Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A. 2016. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nature Communications 7: 13274.
120. Svitashev S, Young JK, Schwartz C, Gao HR, Falco SC, Cigan AM. 2015. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiology 169: 931–945.
121. Tang X, Lowder LG, Zhang T, Malzahn AA, Zheng X, Voytas DF, Zhong Z, Chen Y, Ren Q, Li Q et al. 2017. A CRISPR-Cpf1 system for efficient genome editing and transcriptional repression in plants. Nature Plants 3: 17018.
122. Tang X, Zheng X, Qi Y, Zhang D, Cheng Y, Tang A, Voytas DF, Zhang Y. 2016. A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Molecular Plant 9: 1088–1091.
123. Thakore PI, D’Ippolito AM, Song L, Safi A, Shivakumar NK, Kabadi AM, Reddy TE, Crawford GE, Gersbach CA. 2015. Highly specific epigenome editing by CRISPR-Cas9 repressors for silencing of distal regulatory elements. Nature Methods 12: 1143–1149.
124. Till BJ, Cooper J, Tai TH, Colowit P, Greene EA, Henikoff S, Comai L. 2007. Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biology 7: 19.
125. Tilman D, Balzer C, Hill J, Befort BL. 2011. Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences, USA 108: 20260–20264.
126. Townsend JA, Wright DA, Winfrey RJ, Fu FL, Maeder ML, Joung JK, Voytas DF. 2009. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459: 442–445.
127. Tycko J, Myer VE, Hsu PD. 2016. Methods for optimizing CRISPR-Cas9 genome editing specificity. Molecular Cell 63: 355–370.
128. Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J. 2009. A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biology 9: 115.
129. Ueta R, Abe C, Watanabe T, Sugano SS, Ishihara R, Ezura H, Osakabe Y, Osakabe K. 2017. Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Scientific Reports 7: 507.
130. Waltz E. 2016. CRISPR-edited crops free to enter market, skip regulation. Nature Biotechnology 34: 582.
131. Wang FJ, Wang CL, Liu PQ, Lei CL, Hao W, Gao Y, Liu YG, Zhao KJ. 2016. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the erf transcription factor gene OsERF922. PLoS ONE 11: e0154027.
132. Wang M, Mao Y, Lu Y, Tao X, Zhu J-k. 2017. Multiplex gene editing in rice using the CRISPR-Cpf1 system. Molecular Plant 10: 1011–1013.
133. Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX, Gao CX, Qiu JL. 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology 32: 947–951.
134. Wang Z-P, Xing H-L, Dong L, Zhang H-Y, Han C-Y, Wang X-C, Chen Q-J. 2015. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biology 16: 144.
135. Weber APM, Weber KL, Carr K, Wilkerson C, Ohlrogge JB. 2007. Sampling the Arabidopsis transcriptome with massively parallel pyrosequencing. Plant Physiology 144:32–42.
136. 4 catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria. Proceedings of the National Academy of Sciences, USA 108: 14 688–14 693.
137. Wolter F, Edelmann S, Kadri A, Scholten S. 2017. Characterization of paired Cas9 nickases induced mutations in maize mesophyll protoplasts. Maydica 62: 1–11.
138. Wolter F, Puchta H. 2017. Knocking out consumer concerns and regulator’s rules: efficient use of CRISPR/Cas ribonucleoprotein complexes for genome editing in cereals. Genome Biology 18: 43.
139. Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim S-G, Kim S-T, Choe S, Kim J-S. 2015. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology 33: 1162–1164.
140. Xie K, Minkenberg B, Yang Y. 2015. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proceedings of the National Academy of Sciences, USA 112: 3570–3575.
141. Xie K, Zhang J, Yang Y. 2014. Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Molecular Plant 7: 923–926.
142. Xing H-L, Dong L, Wang Z-P, Zhang H-Y, Han C-Y, Liu B, Wang X-C, Chen Q-J. 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology 14: 327.
143. Yan L, Wei S, Wu Y, Hu R, Li H, Yang W, Xie Q. 2015. High-Efficiency genome editing in Arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Molecular Plant 8: 1820–1823.
144. Ye XD, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I. 2000. Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287: 303–305.
145. Yuan Y, Bayer PE, Batley J, Edwards D. 2017. Improvements in genomic technologies: application to crop genomics. Trends in Biotechnology 35: 547–558.
146. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163: 759–771.
147. Zetsche B, Heidenreich M, Mohanraju P, Fedorova I, Kneppers J, DeGennaro EM, Winblad N, Choudhury SR, Abudayyeh OO, Gootenberg JS et al. 2017. Multiplex gene editing by CRISPR-Cpf1 using a single crRNA array. Nature Biotechnology 35:31–34.
148. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N et al. 2014. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnology Journal 12: 797–807.
149. Zhang WL, Wu YF, Schnable JC, Zeng ZX, Freeling M, Crawford GE, Jiang JM. 2012. High-resolution mapping of open chromatin in the rice genome. Genome Research 22: 151–162.
150. Zhou H, Liu B, Weeks DP, Spalding MH, Yang B. 2014. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Research 42: 10903–10914.
151. Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C. 2017. Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nature Biotechnology 35: 438–440.
152. Zsögön A, Cermak T, Voytas D, Peres LEP. 2017. Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: case study in tomato. Plant Science 256: 120–130.