Many genome editing tools have been developed and new ones are anticipated; some have been extensively applied in plant genetics, biotechnology and breeding, especially the CRISPR/Cas9 system. These technologies have opened up a new era for crop improvement due to their precise editing of user-specified sequences related to agronomic traits. In this review, we will focus on an update of recent developments in the methodologies of editing reagent delivery, and consider the pros and cons of current delivery systems. Finally, we will reflect on possible future directions.
The author(s) declare that they have no conflict of interest.
[1] 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. Sci Rep, 2016, 6: 30910 CrossRef PubMed ADS Google Scholar
[2] Ainley W.M., Sastry-Dent L., Welter M.E., Murray M.G., Zeitler B., Amora R., Corbin D.R., Miles R.R., Arnold N.L., Strange T.L., Simpson M.A., Cao Z., Carroll C., Pawelczak K.S., Blue R., West K., Rowland L.M., Perkins D., Samuel P., Dewes C.M., Shen L., Sriram S., Evans S.L., Rebar E.J., Zhang L., Gregory P.D., Urnov F.D., Webb S.R., Petolino J.F.. Trait stacking via targeted genome editing. Plant Biotechnol J, 2013, 11: 1126-1134 CrossRef PubMed Google Scholar
[3] Ali Z., Abul-faraj A., Li L., Ghosh N., Piatek M., Mahjoub A., Aouida M., Piatek A., Baltes N.J., Voytas D.F., Dinesh-Kumar S., Mahfouz M.M.. Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant, 2015, 8: 1288-1291 CrossRef PubMed Google Scholar
[4] Altpeter F., Springer N.M., Bartley L.E., Blechl A.E., Brutnell T.P., Citovsky V., Conrad L.J., Gelvin S.B., Jackson D.P., Kausch A.P., Lemaux P.G., Medford J.I., Orozco-Cárdenas M.L., Tricoli D.M., Van Eck J., Voytas D.F., Walbot V., Wang K., Zhang Z.J., Stewart C.N.. Advancing crop transformation in the era of genome editing. Plant Cell, 2016, 28: 1510-1520 CrossRef PubMed Google Scholar
[5]
Andersson
M.,
Turesson
H.,
Nicolia
A.,
F?lt
A.S.,
Samuelsson
M.,
Hofvander
P..
Efficient targeted multiallelic mutagenesis in tetraploid potato (
[6] Baltes N.J., Gil-Humanes J., Cermak T., Atkins P.A., Voytas D.F.. DNA replicons for plant genome engineering. Plant Cell, 2014, 26: 151-163 CrossRef PubMed Google Scholar
[7] 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 CrossRef PubMed Google Scholar
[8]
Beetham
P.R.,
Kipp
P.B.,
Sawycky
X.L.,
Arntzen
C.J.,
May
G.D..
A tool for functional plant genomics: chimeric RNA/DNA oligonucleotides cause
[9] Bortesi L., Fischer R.. The CRISPR/Cas9 system for plant genome editing and beyond. Biotech Adv, 2015, 33: 41-52 CrossRef PubMed Google Scholar
[10] Brooks C., Nekrasov V., Lippman Z.B., Van Eck J.. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol, 2014, 166: 1292-1297 CrossRef PubMed Google Scholar
[11]
Butler
N.M.,
Atkins
P.A.,
Voytas
D.F.,
Douches
D.S..
Generation and inheritance of targeted mutations in potato (
[12] Cai Y., Chen L., Liu X., Sun S., Wu C., Jiang B., Han T., Hou W.. CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS ONE, 2015, 10: e0136064 CrossRef PubMed ADS Google Scholar
[13] Cai C.Q., Doyon Y., Ainley W.M., Miller J.C., Dekelver R.C., Moehle E.A., Rock J.M., Lee Y.L., Garrison R., Schulenberg L., Blue R., Worden A., Baker L., Faraji F., Zhang L., Holmes M.C., Rebar E.J., Collingwood T.N., Rubin-Wilson B., Gregory P.D., Urnov F.D., Petolino J.F.. Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol, 2009, 69: 699-709 CrossRef PubMed Google Scholar
[14] Cao M.X., Huang J.Q., Yao Q.H., Liu S.J., Wang C.L., Wei Z.M.. Site-specific DNA excision in transgenic rice with a cell-permeable cre recombinase. Mol Biotechnol, 2006, 32: 055-064 CrossRef Google Scholar
[15] ?ermák T., Baltes N.J., ?egan R., Zhang Y., Voytas D.F.. High-frequency, precise modification of the tomato genome. Genome Biol, 2015, 16: 232 CrossRef PubMed Google Scholar
[16] 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, 17: 1140-1153 CrossRef PubMed Google Scholar
[17] Char S.N., Unger-Wallace E., Frame B., Briggs S.A., Main M., Spalding M.H., Vollbrecht E., Wang K., Yang B.. Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J, 2015, 13: 1002-1010 CrossRef PubMed Google Scholar
[18] Chugh A., Eudes F., Shim Y.S.. Cell-penetrating peptides: nanocarrier for macromolecule delivery in living cells. IUBMB Life, 2010, 62: 183-193 CrossRef PubMed Google Scholar
[19] Clasen B.M., Stoddard T.J., Luo S., Demorest Z.L., Li J., Cedrone F., Tibebu R., Davison S., Ray E.E., Daulhac A., Coffman A., Yabandith A., Retterath A., Haun W., Baltes N.J., Mathis L., Voytas D.F., Zhang F.. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J, 2016, 14: 169-176 CrossRef PubMed Google Scholar
[20] Cole-Strauss A., Yoon K., Xiang Y., Byrne B.C., Rice M.C., Gryn J., Holloman W.K., Kmiec E.B.. Correction of the mutation responsible for sickle cell anemia by an RNA-DNA oligonucleotide. Science, 1996, 273: 1386-1389 CrossRef ADS Google Scholar
[21] Curtin S.J., Zhang F., Sander J.D., Haun W.J., Starker C., Baltes N.J., Reyon D., Dahlborg E.J., Goodwin M.J., Coffman A.P., Dobbs D., Joung J.K., Voytas D.F., Stupar R.M.. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol, 2011, 156: 466-473 CrossRef PubMed Google Scholar
[22]
de Pater
S.,
Neuteboom
L.W.,
Pinas
J.E.,
Hooykaas
P.J.J.,
van der Zaal
B.J..
ZFN-induced mutagenesis and gene-targeting in
[23]
de Pater
S.,
Pinas
J.E.,
Hooykaas
P.J.J.,
van der Zaal
B.J..
ZFN-mediated gene targeting of the
[24] Dinesh-Kumar, S.P., Anandalakshmi, R., Marathe, R., Schiff, M., and Liu, Y. (2003). Virus-induced gene silencing. Methods Mol Biol 236, 287–294. Google Scholar
[25] Dong C., Beetham P., Vincent K., Sharp P.. Oligonucleotide-directed gene repair in wheat using a transient plasmid gene repair assay system. Plant Cell Rep, 2006, 25: 457-465 CrossRef PubMed Google Scholar
[26] Du J., Jin J., Yan M., Lu Y.. Synthetic nanocarriers for intracellular protein delivery. Curr Drug Metab, 2012, 13: 82-92 CrossRef Google Scholar
[27] 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 Biotech, 2016, 217: 90-97 CrossRef PubMed Google Scholar
[28] English J., Davenport G., Elmayan T., Vaucheret H., Baulcombe D.. Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J, 1997, 12: 597-603 CrossRef Google Scholar
[29] 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 CrossRef PubMed ADS Google Scholar
[30]
Fauser
F.,
Schiml
S.,
Puchta
H..
Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in
[31] Feng Z., Zhang B., Ding W., Liu X., Yang D.L., Wei P., Cao F., Zhu S., Zhang F., Mao Y., Zhu J.K.. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res, 2013, 23: 1229-1232 CrossRef PubMed Google Scholar
[32]
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
[33]
Forner
J.,
Pfeiffer
A.,
Langenecker
T.,
Manavella
P.A.,
Manavella
P.,
Lohmann
J.U..
Germline-transmitted genome editing in
[34] Forsyth A., Weeks T., Richael C., Duan H.. Transcription activator-like effector nucleases (TALEN)-mediated targeted DNA insertion in potato plants. Front Plant Sci, 2016, 7: 1572 CrossRef PubMed Google Scholar
[35]
Gao
J.,
Wang
G.,
Ma
S.,
Xie
X.,
Wu
X.,
Zhang
X.,
Wu
Y.,
Zhao
P.,
Xia
Q..
CRISPR/Cas9-mediated targeted mutagenesis in
[36]
Gelvin
S.B..
[37] 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, 2017, 89: 1251-1262 CrossRef PubMed Google Scholar
[38]
Gupta
M.,
DeKelver
R.C.,
Palta
A.,
Clifford
C.,
Gopalan
S.,
Miller
J.C.,
Novak
S.,
Desloover
D.,
Gachotte
D.,
Connell
J.,
Flook
J.,
Patterson
T.,
Robbins
K.,
Rebar
E.J.,
Gregory
P.D.,
Urnov
F.D.,
Petolino
J.F..
Transcriptional activation of
[39] Gurushidze M., Hensel G., Hiekel S., Schedel S., Valkov V., Kumlehn J.. True-breeding targeted gene knock-out in barley using designer TALE-nuclease in haploid cells. PLoS ONE, 2014, 9: e92046 CrossRef PubMed ADS Google Scholar
[40] Hartung F., Schiemann J.. Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J, 2014, 78: 742-752 CrossRef PubMed Google Scholar
[41] Haun W., Coffman A., Clasen B.M., Demorest Z.L., Lowy A., Ray E., Retterath A., Stoddard T., Juillerat A., Cedrone F., Mathis L., Voytas D.F., Zhang F.. Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J, 2014, 12: 934-940 CrossRef PubMed Google Scholar
[42] Huang Y.W., Lee H.J., Tolliver L.M., Aronstam R.S.. Delivery of nucleic acids and nanomaterials by cell-penetrating peptides: opportunities and challenges. BioMed Res Int, 2015, 2015: 1-16 CrossRef PubMed Google Scholar
[43] 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, 2015, 467: 76-82 CrossRef PubMed Google Scholar
[44] Jacobs T.B., LaFayette P.R., Schmitz R.J., Parrott W.A.. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol, 2015, 15: 16 CrossRef PubMed Google Scholar
[45] Jensen, S.P., Febres, V.J., and Moore, G.A. (2014). Cell penetrating peptides as an alternative transformation method in citrus. J Citrus Pathol 1, 10.15. Google Scholar
[46] Jia H., Wang N.. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE, 2014a, 9: e93806 CrossRef PubMed ADS Google Scholar
[47] Jia H., Wang N.. Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Rep, 2014b, 33: 1993-2001 CrossRef PubMed Google Scholar
[48] Jia H., Orbovic V., Jones J.B., Wang N.. Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4:dCsLOB1.3 infection. Plant Biotechnol J, 2016, 14: 1291-1301 CrossRef PubMed Google Scholar
[49]
Jiang
W.,
Zhou
H.,
Bi
H.,
Fromm
M.,
Yang
B.,
Weeks
D.P..
Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in
[50]
Jiang
W.Z.,
Yang
B.,
Weeks
D.P..
Efficient CRISPR/Cas9-mediated gene editing in
[51] Jung J.H., Altpeter F.. TALEN mediated targeted mutagenesis of the caffeic acid O-methyltransferase in highly polyploid sugarcane improves cell wall composition for production of bioethanol. Plant Mol Biol, 2016, 92: 131-142 CrossRef PubMed Google Scholar
[52]
Kapila
J.,
De Rycke
R.,
Van Montagu
M.,
Angenon
G..
An
[53] Kelley M.L., Strezoska , He K., Vermeulen A., Smith A.B.. Versatility of chemically synthesized guide RNAs for CRISPR-Cas9 genome editing. J Biotech, 2016, 233: 74-83 CrossRef PubMed Google Scholar
[54] Kumagai M.H., Donson J., della-Cioppa G., Harvey D., Hanley K., Grill L.K.. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc Natl Acad Sci USA, 1995, 92: 1679-1683 CrossRef ADS Google Scholar
[55]
Lawrenson
T.,
Shorinola
O.,
Stacey
N.,
Li
C.,
?stergaard
L.,
Patron
N.,
Uauy
C.,
Harwood
W..
Induction of targeted, heritable mutations in barley and
[56]
Li
J.F.,
Norville
J.E.,
Aach
J.,
McCormack
M.,
Zhang
D.,
Bush
J.,
Church
G.M.,
Sheen
J..
Multiplex and homologous recombination-mediated genome editing in
[57]
Li
J.,
Stoddard
T.J.,
Demorest
Z.L.,
Lavoie
P.O.,
Luo
S.,
Clasen
B.M.,
Cedrone
F.,
Ray
E.E.,
Coffman
A.P.,
Daulhac
A.,
Yabandith
A.,
Retterath
A.J.,
Mathis
L.,
Voytas
D.F.,
D’Aoust
M.A.,
Zhang
F..
Multiplexed, targeted gene editing in
[58] Li T., Liu B., Spalding M.H., Weeks D.P., Yang B.. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 2012, 30: 390-392 CrossRef PubMed Google Scholar
[59] Li T., Liu B., Chen C.Y., Yang B.. TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice. J Genet Genomics, 2016, 43: 297-305 CrossRef PubMed Google Scholar
[60] Li Z., Liu Z.B., Xing A., Moon B.P., Koellhoffer J.P., Huang L., Ward R.T., Clifton E., Falco S.C., Cigan A.M.. Cas9-guide RNA directed genome editing in soybean. Plant Physiol, 2015, 169: 960-970 CrossRef PubMed Google Scholar
[61]
Liang
Z.,
Zhang
K.,
Chen
K.,
Gao
C..
Targeted mutagenesis in
[62] Liang Z., Chen K., Li T., Zhang Y., Wang Y., Zhao Q., Liu J., Zhang H., Liu C., Ran Y., Gao C.. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun, 2017, 8: 14261 CrossRef PubMed ADS Google Scholar
[63]
Lloyd
A.,
Plaisier
C.L.,
Carroll
D.,
Drews
G.N..
Targeted mutagenesis using zinc-finger nucleases in
[64]
Lor
V.S.,
Starker
C.G.,
Voytas
D.F.,
Weiss
D.,
Olszewski
N.E..
Targeted mutagenesis of the tomato
[65]
Lowe
K.,
Wu
E.,
Wang
N.,
Hoerster
G.,
Hastings
C.,
Cho
M.J.,
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.M.,
Bruce
W.,
Newman
L.,
Shen
B.,
Zheng
P.,
Bidney
D.,
Falco
S.C.,
RegisterIII
J.C.,
Zhao
Z.Y.,
Xu
D.,
Jones
T.J.,
Gordon-Kamm
W.J..
Morphogenic regulators
[66] Luo S., Li J., Stoddard T.J., Baltes N.J., Demorest Z.L., Clasen B.M., Coffman A., Retterath A., Mathis L., Voytas D.F., Zhang F.. Non-transgenic plant genome editing using purified sequence-specific nucleases. Mol Plant, 2015, 8: 1425-1427 CrossRef PubMed Google Scholar
[67] 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 Y.G.. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicotplants. Mol Plant, 2015, 8: 1274-1284 CrossRef PubMed Google Scholar
[68]
Mahfouz
M.M.,
Li
L.,
Shamimuzzaman
M.,
Wibowo
A.,
Fang
X.,
Zhu
J.K..
[69] Malnoy M., Viola R., Jung M.H., Koo O.J., Kim S., Kim J.S., Velasco R., Nagamangala Kanchiswamy C.. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci, 2016, 7: 1904 CrossRef PubMed Google Scholar
[70] Mao Y., Zhang H., Xu N., Zhang B., Gou F., Zhu J.K.. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant, 2013, 6: 2008-2011 CrossRef PubMed Google Scholar
[71] Martin-Ortigosa S., Valenstein J.S., Lin V.S.Y., Trewyn B.G., Wang K.. Gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method. Adv Funct Mater, 2012, 22: 3576-3582 CrossRef Google Scholar
[72] Martin-Ortigosa S., Peterson D.J., Valenstein J.S., Lin V.S.Y., Trewyn B.G., Lyznik L.A., Wang K.. Mesoporous silica nanoparticle-mediated intracellular Cre protein delivery for maize genome editing via loxP site excision. Plant Physiol, 2014, 164: 537-547 CrossRef PubMed Google Scholar
[73] Marton I., Zuker A., Shklarman E., Zeevi V., Tovkach A., Roffe S., Ovadis M., Tzfira T., Vainstein A.. Nontransgenic genome modification in plant cells. Plant Physiol, 2010, 154: 1079-1087 CrossRef PubMed Google Scholar
[74] Miao J., Guo D., Zhang J., Huang Q., Qin G., Zhang X., Wan J., Gu H., Qu L.J.. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res, 2013, 23: 1233-1236 CrossRef PubMed Google Scholar
[75] 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 CrossRef PubMed Google Scholar
[76] Mikami M., Toki S., Endo M.. Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant Cell Physiol, 2016, 57: 1058-1068 CrossRef PubMed Google Scholar
[77]
Nekrasov
V.,
Staskawicz
B.,
Weigel
D.,
Jones
J.D.G.,
Kamoun
S..
Targeted mutagenesis in the model plant
[78] Nicolia A., Proux-Wéra E., ?hman I., Onkokesung N., Andersson M., Andreasson E., Zhu L.H.. Targeted gene mutation in tetraploid potato through transient TALEN expression in protoplasts. J Biotech, 2015, 204: 17-24 CrossRef PubMed Google Scholar
[79] Okuzaki A., Toriyama K.. Chimeric RNA/DNA oligonucleotide-directed gene targeting in rice. Plant Cell Rep, 2004, 22: 509-512 CrossRef PubMed Google Scholar
[80]
Osakabe
K.,
Osakabe
Y.,
Toki
S..
Site-directed mutagenesis in
[81] Paul J.W., Qi Y.. CRISPR/Cas9 for plant genome editing: accomplishments, problems and prospects. Plant Cell Rep, 2016, 35: 1417-1427 CrossRef PubMed Google Scholar
[82] Peer R., Rivlin G., Golobovitch S., Lapidot M., Gal-On A., Vainstein A., Tzfira T., Flaishman M.A.. Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees. Planta, 2015, 241: 941-951 CrossRef PubMed Google Scholar
[83] Petolino J.F.. Genome editing in plants via designed zinc finger nucleases. Cell Dev Biol-Plant, 2015, 51: 1-8 CrossRef PubMed Google Scholar
[84]
Piatek
A.,
Ali
Z.,
Baazim
H.,
Li
L.,
Abulfaraj
A.,
Al-Shareef
S.,
Aouida
M.,
Mahfouz
M.M..
RNA-guided transcriptional regulation
[85] Popat A., Hartono S.B., Stahr F., Liu J., Qiao S.Z., Qing (Max) Lu G.. Mesoporous silica nanoparticles for bioadsorption, enzyme immobilisation, and delivery carriers. Nanoscale, 2011, 3: 2801-2818 CrossRef PubMed ADS Google Scholar
[86]
Pratt, S. Growers to see new HT canola in 2016. The Western Producer. 2012-05-28.
[87]
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
[88]
Qi
Y.,
Li
X.,
Zhang
Y.,
Starker
C.G.,
Baltes
N.J.,
Zhang
F.,
Sander
J.D.,
Reyon
D.,
Joung
J.K.,
Voytas
D.F..
Targeted deletion and inversion of tandemly arrayed genes in
[89] Raitskin O., Patron N.J.. Multi-gene engineering in plants with RNA-guided Cas9 nuclease. Curr Opin Biotech, 2016, 37: 69-75 CrossRef PubMed Google Scholar
[90] Rakoczy-Trojanowska, M. (2002). Alternative methods of plant transformation: a short review. Cell Mol Biol Lett 7, 849–858. Google Scholar
[91]
Ren
C.,
Liu
X.,
Zhang
Z.,
Wang
Y.,
Duan
W.,
Li
S.,
Liang
Z..
CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (
[92] Rinaldo A.R., Ayliffe M.. Gene targeting and editing in crop plants: a new era of precision opportunities. Mol Breeding, 2015, 35: 40 CrossRef Google Scholar
[93] Sauer N.J., Narváez-Vásquez J., Mozoruk J., Miller R.B., Warburg Z.J., Woodward M.J., Mihiret Y.A., Lincoln T.A., Segami R.E., Sanders S.L., Walker K.A., Beetham P.R., Sch?pke C.R., Gocal G.F.W.. Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol, 2016, 170: 1917-1928 CrossRef PubMed Google Scholar
[94] Schaeffer S.M., Nakata P.A.. CRISPR/Cas9-mediated genome editing and gene replacement in plants: transitioning from lab to field. Plant Sci, 2015, 240: 130-142 CrossRef PubMed Google Scholar
[95]
Schiml
S.,
Fauser
F.,
Puchta
H..
The CRISPR/Cas system can be used as nuclease for
[96]
Shan
Q.,
Wang
Y.,
Chen
K.,
Liang
Z.,
Li
J.,
Zhang
Y.,
Zhang
K.,
Liu
J.,
Voytas
D.F.,
Zheng
X.,
Zhang
Y.,
Gao
C..
Rapid and efficient gene modification in rice and
[97] 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, 2013b, 31: 686-688 CrossRef PubMed Google Scholar
[98]
Shan
Q.,
Zhang
Y.,
Chen
K.,
Zhang
K.,
Gao
C..
Creation of fragrant rice by targeted knockout of the
[99] 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, 2017, 15: 207-216 CrossRef PubMed Google Scholar
[100]
Shukla
V.K.,
Doyon
Y.,
Miller
J.C.,
DeKelver
R.C.,
Moehle
E.A.,
Worden
S.E.,
Mitchell
J.C.,
Arnold
N.L.,
Gopalan
S.,
Meng
X.,
Choi
V.M.,
Rock
J.M.,
Wu
Y.Y.,
Katibah
G.E.,
Zhifang
G.,
McCaskill
D.,
Simpson
M.A.,
Blakeslee
B.,
Greenwalt
S.A.,
Butler
H.J.,
Hinkley
S.J.,
Zhang
L.,
Rebar
E.J.,
Gregory
P.D.,
Urnov
F.D..
Precise genome modification in the crop species
[101] Stoddard T.J., Clasen B.M., Baltes N.J., Demorest Z.L., Voytas D.F., Zhang F., Luo S.. Targeted mutagenesis in plant cells through transformation of sequence-specific nuclease mRNA. PLoS ONE, 2016, 11: e0154634 CrossRef PubMed ADS Google Scholar
[102]
Sugano
S.S.,
Shirakawa
M.,
Takagi
J.,
Matsuda
Y.,
Shimada
T.,
Hara-Nishimura
I.,
Kohchi
T..
CRISPR/Cas9-mediated targeted mutagenesis in the liverwort
[103] Sun X., Hu Z., Chen R., Jiang Q., Song G., Zhang H., Xi Y.. Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep, 2015, 5: 10342 CrossRef PubMed ADS Google Scholar
[104] Svitashev S., Young J.K., Schwartz C., Gao H., Falco S.C., Cigan A.M.. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol, 2015, 169: 931-945 CrossRef PubMed Google Scholar
[105] Svitashev S., Schwartz C., Lenderts B., Young J.K., Mark Cigan A.. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun, 2016, 7: 13274 CrossRef PubMed ADS Google Scholar
[106] Torney F., Trewyn B.G., Lin V.S.Y., Wang K.. Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotech, 2007, 2: 295-300 CrossRef PubMed ADS Google Scholar
[107] Tovkach A., Zeevi V., Tzfira T.. A toolbox and procedural notes for characterizing novel zinc finger nucleases for genome editing in plant cells. Plant J, 2009, 57: 747-757 CrossRef PubMed Google Scholar
[108] Townsend J.A., Wright D.A., Winfrey R.J., Fu F., Maeder M.L., Joung J.K., Voytas D.F.. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 2009, 459: 442-445 CrossRef PubMed ADS Google Scholar
[109] Upadhyay S.K., Kumar J., Alok A., Tuli R.. RNA-guided genome editing for target gene mutations in wheat. G3, 2013, 3: 2233-2238 CrossRef PubMed Google Scholar
[110] Vainstein A., Marton I., Zuker A., Danziger M., Tzfira T.. Permanent genome modifications in plant cells by transient viral vectors. Trends Biotech, 2011, 29: 363-369 CrossRef PubMed Google Scholar
[111] Voytas D.F., Gao C.. Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol, 2014, 12: e1001877 CrossRef PubMed Google Scholar
[112] Wang S., Zhang S., Wang W., Xiong X., Meng F., Cui X.. Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep, 2015, 34: 1473-1476 CrossRef PubMed Google Scholar
[113]
Wang
L.,
Li
F.,
Dang
L.,
Liang
C.,
Wang
C.,
He
B.,
Liu
J.,
Li
D.,
Wu
X.,
Xu
X.,
Lu
A.,
Zhang
G..
[114]
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
[115] Wang Y., Cheng X., Shan Q., Zhang Y., Liu J., Gao C., Qiu J.L.. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 2014, 32: 947-951 CrossRef PubMed Google Scholar
[116]
Wang
Z.P.,
Xing
H.L.,
Dong
L.,
Zhang
H.Y.,
Han
C.Y.,
Wang
X.C.,
Chen
Q.J..
Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in
[117] Weeks D.P., Spalding M.H., Yang B.. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J, 2016, 14: 483-495 CrossRef PubMed Google Scholar
[118] Wendt T., Holm P.B., Starker C.G., Christian M., Voytas D.F., Brinch-Pedersen H., Holme I.B.. TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol, 2013, 83: 279-285 CrossRef PubMed Google Scholar
[119] Weinthal D., Tovkach A., Zeevi V., Tzfira T.. Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci, 2010, 15: 308-321 CrossRef PubMed Google Scholar
[120] Woo J.W., Kim J., Kwon S.I., Corvalán C., Cho S.W., Kim H., Kim S.G., Kim S.T., Choe S., Kim J.S.. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol, 2015, 33: 1162-1164 CrossRef PubMed Google Scholar
[121] Wright D.A., Townsend J.A., Winfrey Jr R.J., Irwin P.A., Rajagopal J., Lonosky P.M., Hall B.D., Jondle M.D., Voytas D.F.. High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J, 2005, 44: 693-705 CrossRef PubMed Google Scholar
[122] Xie K., Yang Y.. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant, 2013, 6: 1975-1983 CrossRef PubMed Google Scholar
[123] 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 CrossRef PubMed ADS Google Scholar
[124] Xing H.L., Dong L., Wang Z.P., Zhang H.Y., Han C.Y., Liu B., Wang X.C., Chen Q.J.. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol, 2014, 14: 327 CrossRef PubMed Google Scholar
[125]
Xu
R.,
Li
H.,
Qin
R.,
Wang
L.,
Li
L.,
Wei
P.,
Yang
J..
Gene targeting using the
[126]
Yan
L.,
Wei
S.,
Wu
Y.,
Hu
R.,
Li
H.,
Yang
W.,
Xie
Q..
High-efficiency genome editing in
[127] 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, 2015, 5: 14926 CrossRef PubMed ADS Google Scholar
[128] Yoon K., Cole-Strauss A., Kmiec E.B.. Targeted gene correction of episomal DNA in mammalian cells mediated by a chimeric RNA.DNA oligonucleotide. Proc Natl Acad Sci USA, 1996, 93: 2071-2076 CrossRef Google Scholar
[129]
Zhang
F.,
Maeder
M.L.,
Unger-Wallace
E.,
Hoshaw
J.P.,
Reyon
D.,
Christian
M.,
Li
X.,
Pierick
C.J.,
Dobbs
D.,
Peterson
T.,
Joung
J.K.,
Voytas
D.F..
High frequency targeted mutagenesis in
[130] Zhang H., Zhang J., Wei P., Zhang B., Gou F., Feng Z., Mao Y., Yang L., Zhang H., Xu N., Zhu J.K.. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J, 2014, 12: 797-807 CrossRef PubMed Google Scholar
[131] Zhang H., Gou F., Zhang J., Liu W., Li Q., Mao Y., Botella J.R., Zhu J.K.. TALEN-mediated targeted mutagenesis produces a large variety of heritable mutations in rice. Plant Biotechnol J, 2016, 14: 186-194 CrossRef PubMed Google Scholar
[132] Zhang Y., Zhang F., Li X., Baller J.A., Qi Y., Starker C.G., Bogdanove A.J., Voytas D.F.. Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol, 2013, 161: 20-27 CrossRef PubMed Google Scholar
[133] 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, 2016, 7: 12617 CrossRef PubMed ADS Google Scholar
[134] Zhou H., Liu B., Weeks D.P., Spalding M.H., Yang B.. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res, 2014, 42: 10903-10914 CrossRef PubMed Google Scholar
[135]
Zhu
T.,
Peterson
D.J.,
Tagliani
L.,
St. Clair
G.,
Baszczynski
C.L.,
Bowen
B..
Targeted manipulation of maize genes
[136] Zhu T., Mettenburg K., Peterson D.J., Tagliani L., Baszczynski C.L.. Engineering herbicide-resistant maize using chimeric RNA/DNA oligonucleotides. Nat Biotechnol, 2000, 18: 555-558 CrossRef PubMed Google Scholar
Figure 1
General procedure for genome editing in plants.
Figure 2
Construct design for ZFNs, TALENs and CRISPR/Cas9 when
Plant species/Editor/Targeted gene(s) |
Targeted outcome |
Delivery method for transient assay or stable edited cells |
Delivery method for stable events |
Reference |
Deletion, replacement and insertion (Multiplex) |
Protoplast transfection, |
|||
Deletion and insertion |
Agroinfiltration |
|||
Deletion and insertion |
Floral dipping |
|||
Deletion and insertion |
Protoplast transfection |
|||
Deletion and insertion |
||||
Deletion, replacement (HDR, NHEJ) and insertion (Multiplex) |
Protoplast transfection |
|||
Replacement (HDR) |
Floral dipping |
|||
Deletion and insertion |
Floral dipping |
|||
Deletion and insertion |
Floral dipping |
|||
Deletion and insertion. (HR- |
Floral dipping |
|||
Deletion and insertion (Multiplex) |
Floral dipping |
|||
Deletion and insertion |
Floral dipping |
|||
Deletion, replacement (HDR, NHEJ) and insertion |
Protoplast transfection, |
|||
Deletion |
Agroinfiltration |
|||
Deletion |
Agroinfiltration |
|||
Deletion |
Agroinfiltration |
|||
Regulation |
Agroinfiltration |
|||
Deletion and insertion |
TRV-mediated transformation |
|||
Deletion and insertion (NHEJ) |
Agroinfiltration |
|||
Deletion and insertion |
Agro-geminivirus |
|||
Deletion and insertion |
Protoplast transfection |
|||
Deletion and insertion |
Agro-geminivirus |
|||
Deletion and insertion |
||||
Deletion and insertion (NHEJ) |
Protoplast transfection |
|||
Deletion and insertion |
Agoinfiltration |
|||
Deletion, replacement (HDR, NHEJ) and insertion |
Protoplast transfection |
Biolistic delivery |
||
Deletion and insertion |
Protoplast transfection |
|||
Deletion and insertion |
Protoplast transfection |
|||
Deletion |
||||
Deletion and insertion (individual and multiplex) |
||||
Replacement |
||||
Deletion, substitution (HDR, NHEJ) and insertion |
||||
Deletion and insertion -large deletion (245 kb) |
Protoplast transfection |
|||
Deletion, substitution (HDR, NHEJ) and insertion |
||||
( |
a)At,
Copyright 2019 Science China Press Co., Ltd. 科学大众杂志社有限责任公司 版权所有
京ICP备18024590号-1