Applications and roles of the CRISPR system in genome editing of plants

Wei Tang , Anna Y. Tang

Journal of Forestry Research ›› 2016, Vol. 28 ›› Issue (1) : 15 -28.

PDF
Journal of Forestry Research ›› 2016, Vol. 28 ›› Issue (1) : 15 -28. DOI: 10.1007/s11676-016-0281-7
Review Article

Applications and roles of the CRISPR system in genome editing of plants

Author information +
History +
PDF

Abstract

Genome editing is a valuable tool to target specific DNA sequences for mutagenesis in the genomes of microbes, plants, and animals. Although different genome editing technologies are available, the clustered regularly interspaced short palindromic repeats/Cas9 (CRISPR/Cas9) system, which utilizes engineered endonucleases to generate a double-stranded DNA break (DSB) in the target DNA region and subsequently stimulates site-specific mutagenesis through DNA repair machineries, is emerging as a powerful genome editing tool for elucidating mechanisms of protection from plant viruses, plant disease resistance, and gene functions in basic and applied research. In this review, we provide an overview of recent advances in the CRISPR system associated genome editing in plants by focusing on application of this technology in model plants, crop plants, fruit plants, woody plants and grasses and discuss how genome editing associated with the CRISPR system can provide insights into genome modifications and functional genomics in plants.

Keywords

CRISPR system / Double-stranded DNA break / Functional genomics / Genome editing / Genome modifications

Cite this article

Download citation ▾
Wei Tang, Anna Y. Tang. Applications and roles of the CRISPR system in genome editing of plants. Journal of Forestry Research, 2016, 28(1): 15-28 DOI:10.1007/s11676-016-0281-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Acevedo-Garcia J, Kusch S, Panstruga R. Magical mystery tour: mLO proteins in plant immunity and beyond. New Phytol, 2014, 204: 273-281.

[2]

Ali Z, Abul-Faraj A, Piatek M, Mahfouz MM. Activity and specificity of TRV-mediated gene editing in plants. Plant Signal Behav, 2015, 10: e1044191.

[3]

Baltes NJ, Voytas DF. Enabling plant synthetic biology through genome engineering. Trends Biotechnol, 2015, 33: 120-131.

[4]

Basak J, Nithin C. Targeting Non-Coding RNAs in plants with the CRISPR-Cas technology is a challenge yet worth accepting. Front Plant Sci, 2015, 6: 1001.

[5]

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.

[6]

Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V. Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol, 2015, 32: 76-84.

[7]

Bogdanove AJ. Principles and applications of TAL effectors for plant physiology and metabolism. Curr Opin Plant Biol, 2014, 19: 99-104.

[8]

Bortesi L, Fischer R. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv, 2015, 33: 41-52.

[9]

Butler NM, Atkins PA, Voytas DF, Douches DS. Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) Using the CRISPR/Cas system. PLoS ONE, 2015, 10: e0144591.

[10]

Cermak T, Baltes NJ, Cegan R, Zhang Y, Voytas DF. High-frequency, precise modification of the tomato genome. Genome Biol, 2015, 16: 232.

[11]

Chandrasegaran S, Carroll D. Origins of programmable nucleases for genome engineering. J Mol Biol, 2015, 33: 543-548.

[12]

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, 2016

[13]

Chaparro-Garcia A, Kamoun S, Nekrasov V. Boosting plant immunity with CRISPR/Cas. Genome Biol, 2015, 16: 254.

[14]

Du H, Zeng X, Zhao M, Cui X, Wang Q, Yang H, Cheng H, Yu D. Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J Biotechnol, 2016, 217: 90-97.

[15]

Duan YB, Li J, Qin RY, Xu RF, Li H, Yang YC, Ma H, Li L, Wei PC, Yang JB. Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol Biol, 2015, 90(1–2): 49-62.

[16]

Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K. Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep, 2015, 5: 12217.

[17]

Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci U S A, 2014, 111: 4632-4637.

[18]

Fichtner F, Urrea Castellanos R, Ulker B. Precision genetic modifications: a new era in molecular biology and crop improvement. Planta, 2014, 239: 921-939.

[19]

Frampton RA, Pitman AR, Fineran PC. Advances in bacteriophage-mediated control of plant pathogens. Int J Microbiol, 2012, 2012: 326452.

[20]

Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q. CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol, 2015, 87: 99-110.

[21]

Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y. Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci USA, 2015, 112: 2275-2280.

[22]

Hyun Y, Kim J, Cho SW, Choi Y, Kim JS, Coupland G. Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta, 2015, 241: 271-284.

[23]

Ilardi V, Tavazza M. Biotechnological strategies and tools for Plum pox virus resistance: trans-, intra-, cis-genesis, and beyond. Front Plant Sci, 2015, 6: 379.

[24]

Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol, 2015, 15: 16.

[25]

Jameson PE, Song J. Cytokinin: a key driver of seed yield. J Exp Bot, 2015, 67: 593-606.

[26]

Jia H, Wang N. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE, 2014, 9: e93806.

[27]

Jia H, Wang N. Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Rep, 2014, 33: 1993-2001.

[28]

Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res, 2013, 41: e188.

[29]

Jiang W, Yang B, Weeks DP. Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE, 2014, 9: e99225.

[30]

Johnson RA, Gurevich V, Filler S, Samach A, Levy AA. Comparative assessments of CRISPR-Cas nucleases’ cleavage efficiency in planta. Plant Mol Biol, 2015, 87: 143-156.

[31]

Kumar V, Jain M. The CRISPR-Cas system for plant genome editing: advances and opportunities. J Exp Bot, 2015, 66: 47-57.

[32]

Li JF, Zhang D, Sheen J. Cas9-based genome editing in Arabidopsis and tobacco. Methods Enzymol, 2014, 546: 459-472.

[33]

Liang Z, Zhang K, Chen K, Gao C. Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics, 2014, 41: 63-68.

[34]

Lowder LG, Zhang D, Baltes NJ, Paul JW 3rd, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol, 2015, 169: 971-985.

[35]

Lozano-Juste J, Cutler SR. Plant genome engineering in full bloom. Trends Plant Sci, 2014, 19: 284-287.

[36]

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu YG. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant, 2015, 8: 1274-1284.

[37]

Mahfouz MM, Piatek A, Stewart CN Jr. Genome engineering via TALENs and CRISPR/Cas9 systems: challenges and perspectives. Plant Biotechnol J, 2014, 12: 1006-1014.

[38]

Michno JM, Wang X, Liu J, Curtin SJ, Kono TJ, Stupar RM. CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops Food, 2015, 6: 243-252.

[39]

Mikami M, Toki S, Endo M. Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol Biol, 2015, 88: 561-572.

[40]

Mikami M, Toki S, Endo M. Parameters affecting frequency of CRISPR/Cas9 mediated targeted mutagenesis in rice. Plant Cell Rep, 2015, 34: 1807-1815.

[41]

Nagamangala Kanchiswamy C, Sargent DJ, Velasco R, Maffei ME, Malnoy M. Looking forward to genetically edited fruit crops. Trends Biotechnol, 2015, 33: 62-64.

[42]

Nejat N, Rookes J, Mantri NL, Cahill DM (2016) Plant-pathogen interactions: toward development of next-generation disease-resistant plants. Crit Rev Biotechnol. doi:10.3109/07388551.2015.1134437

[43]

Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol, 2013, 31: 691-693.

[44]

Nemudryi AA, Valetdinova KR, Medvedev SP, Zakian SM. TALEN and CRISPR/Cas genome editing systems: tools of discovery. Acta Naturae, 2014, 6: 19-40.

[45]

Osakabe Y, Osakabe K. Genome editing with engineered nucleases in plants. Plant Cell Physiol, 2015, 56: 389-400.

[46]

Puchta H, Fauser F. Gene targeting in plants: 25 years later. Int J Dev Biol, 2013, 57: 629-637.

[47]

Quetier F. The CRISPR-Cas9 technology: closer to the ultimate toolkit for targeted genome editing. Plant Sci, 2016, 242: 65-76.

[48]

Richter C, Gristwood T, Clulow JS, Fineran PC. In vivo protein interactions and complex formation in the Pectobacterium atrosepticum subtype I-F CRISPR/Cas system. PLoS ONE, 2012, 7: e49549.

[49]

Ricroch AE, Henard-Damave MC. Next biotech plants: new traits, crops, developers and technologies for addressing global challenges. Crit Rev Biotechnol, 2015, 35: 1-16.

[50]

Sauer NJ, Mozoruk J, Miller RB, Warburg ZJ, Walker KA, Beetham PR, Schopke CR, Gocal GF. Oligonucleotide-directed mutagenesis for precision gene editing. Plant Biotechnol J, 2015, 14(2): 448-462.

[51]

Schaart JG, van de Wiel CC, Lotz LA, Smulders MJ. Opportunities for products of new plant breeding techniques. Trends Plant Sci, 2015, 21(5): 438-449.

[52]

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, 2014, 80: 1139-1150.

[53]

Schuster M, Schweizer G, Reissmann S, Kahmann R. Genome editing in ustilago maydis using the crispr-cas system. Fungal Genet Biol, 2015, 89: 3-9.

[54]

Scott JN, Kupinski AP, Boyes J. Targeted genome regulation and modification using transcription activator-like effectors. FEBS J, 2014, 281: 4583-4597.

[55]

Seo YS, Lim JY, Park J, Kim S, Lee HH, Cheong H, Kim SM, Moon JS, Hwang I. Comparative genome analysis of rice-pathogenic Burkholderia provides insight into capacity to adapt to different environments and hosts. BMC Genom, 2015, 16: 349.

[56]

Shan Q, Wang Y, Li J, Gao C. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc, 2014, 9: 2395-2410.

[57]

Shariat N, Dudley EG. CRISPRs: molecular signatures used for pathogen subtyping. Appl Environ Microbiol, 2014, 80: 430-439.

[58]

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, 2015, 84: 1295-1305.

[59]

Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T. CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol, 2014, 55: 475-481.

[60]

Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and Guide RNA. Plant Physiol, 2015, 169: 931-945.

[61]

Teotia S, Singh D, Tang X, Tang G. Essential RNA-based technologies and their applications in plant functional genomics. Trends Biotechnol, 2016, 34: 106-123.

[62]

Trevino AE, Zhang F. Genome editing using Cas9 nickases. Methods Enzymol, 2014, 546: 161-174.

[63]

Tsai CJ, Xue LJ. CRISPRing into the woods. GM Crops Food, 2015, 6: 206-215.

[64]

Upadhyay SK, Kumar J, Alok A, Tuli R. RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda), 2013, 3(12): 2233-2238.

[65]

Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 2014, 32: 947-951.

[66]

Wang M, Liu Y, Zhang C, Liu J, Liu X, Wang L, Wang W, Chen H, Wei C, Ye X, Li X, Tu J. Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations. PLoS ONE, 2015, 10: e0122755.

[67]

Weeks DP, Spalding MH, Yang B. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J, 2015, 14(2): 483-495.

[68]

Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol, 2015, 33: 1162-1164.

[69]

Xie K, Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant, 2013, 6: 1975-1983.

[70]

Xie K, Minkenberg B, Yang Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA, 2015, 112: 3570-3575.

[71]

Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol, 2014, 14: 327.

[72]

Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J. Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice (N Y), 2014, 7: 5.

[73]

Yin K, Han T, Liu G, Chen T, Wang Y, Yu AY, Liu Y. A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing. Sci Rep, 2015, 5: 14926.

[74]

Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, Zhu JK. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J, 2014, 12: 797-807.

[75]

Zhang B, Yang X, Yang C, Li M, Guo Y. Exploiting the CRISPR/Cas9 system for targeted genome mutagenesis in petunia. Sci Rep, 2016, 6: 20315.

[76]

Zhang H, Gou F, Zhang J, Liu W, Li Q, Mao Y, Botella JR, Zhu JK. TALEN-mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotechnol J, 2016, 14: 186-194.

[77]

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 Res, 2014, 42: 10903-10914.

[78]

Zlotorynski E. Plant cell biology: cRISPR-Cas protection from plant viruses. Nat Rev Mol Cell Biol, 2015, 16: 642.

AI Summary AI Mindmap
PDF

181

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/