Highly efficient homology‐directed repair using CRISPR/Cpf1‐geminiviral replicon in tomato

Summary Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR‐based genome editing efficiency approximately threefold compared with a Cas9‐based single‐repl...

Full description

Saved in:
Bibliographic Details
Published inPlant biotechnology journal Vol. 18; no. 10; pp. 2133 - 2143
Main Authors Vu, Tien Van, Sivankalyani, Velu, Kim, Eun‐Jung, Doan, Duong Thi Hai, Tran, Mil Thi, Kim, Jihae, Sung, Yeon Woo, Park, Minwoo, Kang, Yang Jae, Kim, Jae‐Yean
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.10.2020
John Wiley and Sons Inc
Subjects
Alleles
Antibiotics
Binding sites
biotechnology
Cell culture
Cloning
CRISPR
CRISPR/Cas9
CRISPR/Cpf1
Deoxyribonucleic acid
DNA
Editing
Efficiency
gene targeting
Genetic transformation
genome editing
Genomes
genomics
Germination
Heredity
Homology
homology‐directed repair
multi‐replicon
Mutation
Non-homologous end joining
Offspring
phenotypic selection
Plant cells
progeny
Proteins
Repair
replicon
Reproduction (biology)
salt tolerance
self-pollination
Sodium chloride
temperature
Tomatoes
CRISPR/Cpf1
gene targeting
genome editing
multi-replicon
CRISPR/Cas9
homology-directed repair
Online AccessGet full text

Cover

Abstract Summary Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR‐based genome editing efficiency approximately threefold compared with a Cas9‐based single‐replicon system via the use of de novo multi‐replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon‐free but stable HDR alleles. The efficiency of CRISPR/LbCpf1‐based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium‐mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single‐replicon system into a multi‐replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR‐based genome editing of a salt‐tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self‐pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene‐free editing of alleles of interest in asexually and sexually reproducing plants.
AbstractList Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR‐based genome editing efficiency approximately threefold compared with a Cas9‐based single‐replicon system via the use of de novo multi‐replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon‐free but stable HDR alleles. The efficiency of CRISPR/LbCpf1‐based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium ‐mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single‐replicon system into a multi‐replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR‐based genome editing of a salt‐tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self‐pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 m m NaCl. Our work may pave the way for transgene‐free editing of alleles of interest in asexually and sexually reproducing plants.
Summary Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR‐based genome editing efficiency approximately threefold compared with a Cas9‐based single‐replicon system via the use of de novo multi‐replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon‐free but stable HDR alleles. The efficiency of CRISPR/LbCpf1‐based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium‐mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single‐replicon system into a multi‐replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR‐based genome editing of a salt‐tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self‐pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene‐free editing of alleles of interest in asexually and sexually reproducing plants.
Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR‐based genome editing efficiency approximately threefold compared with a Cas9‐based single‐replicon system via the use of de novo multi‐replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon‐free but stable HDR alleles. The efficiency of CRISPR/LbCpf1‐based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium‐mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single‐replicon system into a multi‐replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR‐based genome editing of a salt‐tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self‐pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene‐free editing of alleles of interest in asexually and sexually reproducing plants.
Genome editing via the homology-directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error-prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR-based genome editing efficiency approximately threefold compared with a Cas9-based single-replicon system via the use of de novo multi-replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon-free but stable HDR alleles. The efficiency of CRISPR/LbCpf1-based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium-mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single-replicon system into a multi-replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR-based genome editing of a salt-tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self-pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene-free editing of alleles of interest in asexually and sexually reproducing plants.Genome editing via the homology-directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error-prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR-based genome editing efficiency approximately threefold compared with a Cas9-based single-replicon system via the use of de novo multi-replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon-free but stable HDR alleles. The efficiency of CRISPR/LbCpf1-based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium-mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single-replicon system into a multi-replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR-based genome editing of a salt-tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self-pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene-free editing of alleles of interest in asexually and sexually reproducing plants.
Genome editing via the homology-directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error-prone repair by nonhomologous end joining (NHEJ). Here, we increased HDR-based genome editing efficiency approximately threefold compared with a Cas9-based single-replicon system via the use of de novo multi-replicon systems equipped with CRISPR/LbCpf1 in tomato and obtained replicon-free but stable HDR alleles. The efficiency of CRISPR/LbCpf1-based HDR was significantly modulated by physical culture conditions such as temperature and light. Ten days of incubation at 31 °C under a light/dark cycle after Agrobacterium-mediated transformation resulted in the best performance among the tested conditions. Furthermore, we developed our single-replicon system into a multi-replicon system that effectively increased HDR efficiency. Although this approach is still challenging, we showed the feasibility of HDR-based genome editing of a salt-tolerant SlHKT1;2 allele without genomic integration of antibiotic markers or any phenotypic selection. Self-pollinated offspring plants carrying the HKT1;2 HDR allele showed stable inheritance and germination tolerance in the presence of 100 mm NaCl. Our work may pave the way for transgene-free editing of alleles of interest in asexually and sexually reproducing plants.
Author Sivankalyani, Velu
Tran, Mil Thi
Park, Minwoo
Sung, Yeon Woo
Kim, Eun‐Jung
Kang, Yang Jae
Kim, Jae‐Yean
Doan, Duong Thi Hai
Vu, Tien Van
Kim, Jihae
AuthorAffiliation 3 Hyundai Seed Co., LTD. Yeoju Korea
2 National Key Laboratory for Plant Cell Biotechnology Agricultural Genetics Institute Bac Tu Liem Vietnam
1 Division of Applied Life Science (BK21 Plus Program) Plant Molecular Biology and Biotechnology Research Center Gyeongsang National University Jinju Korea
4 Division of Life Science Gyeongsang National University Jinju Korea
AuthorAffiliation_xml – name: 3 Hyundai Seed Co., LTD. Yeoju Korea
– name: 1 Division of Applied Life Science (BK21 Plus Program) Plant Molecular Biology and Biotechnology Research Center Gyeongsang National University Jinju Korea
– name: 2 National Key Laboratory for Plant Cell Biotechnology Agricultural Genetics Institute Bac Tu Liem Vietnam
– name: 4 Division of Life Science Gyeongsang National University Jinju Korea
Author_xml – sequence: 1
  givenname: Tien Van
  surname: Vu
  fullname: Vu, Tien Van
  organization: Agricultural Genetics Institute
– sequence: 2
  givenname: Velu
  surname: Sivankalyani
  fullname: Sivankalyani, Velu
  organization: Gyeongsang National University
– sequence: 3
  givenname: Eun‐Jung
  surname: Kim
  fullname: Kim, Eun‐Jung
  organization: Gyeongsang National University
– sequence: 4
  givenname: Duong Thi Hai
  surname: Doan
  fullname: Doan, Duong Thi Hai
  organization: Gyeongsang National University
– sequence: 5
  givenname: Mil Thi
  surname: Tran
  fullname: Tran, Mil Thi
  organization: Gyeongsang National University
– sequence: 6
  givenname: Jihae
  surname: Kim
  fullname: Kim, Jihae
  organization: Gyeongsang National University
– sequence: 7
  givenname: Yeon Woo
  surname: Sung
  fullname: Sung, Yeon Woo
  organization: Gyeongsang National University
– sequence: 8
  givenname: Minwoo
  surname: Park
  fullname: Park, Minwoo
  organization: Hyundai Seed Co., LTD
– sequence: 9
  givenname: Yang Jae
  surname: Kang
  fullname: Kang, Yang Jae
  organization: Gyeongsang National University
– sequence: 10
  givenname: Jae‐Yean
  orcidid: 0000-0002-1180-6232
  surname: Kim
  fullname: Kim, Jae‐Yean
  email: kimjy@gnu.ac.kr
  organization: Gyeongsang National University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32176419$$D View this record in MEDLINE/PubMed
BookMark eNqNks1u1DAUhS1URH9gwQugSGxgMR3_xpMNEoyAjlSJqsAWy3aczK0cO3WSotnxCDwjT4KHmVZQgYQ3tq6_e3SufY7RQYjBIfSU4FOS17w3cEoYk-wBOiK8lDNZCnpwd-b8EB0PwxXGlJSifIQOGSW5TKoj9OUM2rXfFK5pwIILY7GOXfSx3fz49r2G5Ozo6iK5XkMqpgFCWywvVx8vLufLviGZaV0HAW4gab_FPNgYCgjFGDs9xsfoYaP94J7s9xP0-d3bT8uz2fmH96vl6_OZFZyymWaC2YUxTNemLpnWZcmdYbVjpLLYEE6MwQ4v5MJaXVaVoY3kTGhqhMHY1uwEvdrp9pPpXG3zINmQ6hN0Om1U1KD-vAmwVm28UVJwjDnPAi_2AileT24YVQeDdd7r4OI0KCooZ7QS8j9QJmW54BUnGX1-D72KUwr5JRTlnNCKY44z9ex383eub38pA_MdYFMchuQaZWHUI8TtLOAVwWqbA5VzoH7lIHe8vNdxK_o3dq_-Fbzb_BtUF29Wu46f6fvEOQ
CitedBy_id crossref_primary_10_1111_pbi_13426
crossref_primary_10_1111_pbi_13546
crossref_primary_10_1007_s12374_023_09383_8
crossref_primary_10_1016_j_tplants_2021_07_018
crossref_primary_10_1093_hr_uhae294
crossref_primary_10_3389_fpls_2023_1186932
crossref_primary_10_1007_s11240_021_02177_1
crossref_primary_10_1093_hr_uhac154
crossref_primary_10_3389_fpls_2022_868027
crossref_primary_10_5483_BMBRep_2023_0210
crossref_primary_10_1002_biot_202100673
crossref_primary_10_1016_j_ymthe_2023_11_013
crossref_primary_10_1007_s00299_021_02708_2
crossref_primary_10_3389_fpls_2022_883421
crossref_primary_10_3390_foods12193681
crossref_primary_10_1002_cpz1_608
crossref_primary_10_1093_pcp_pcab123
crossref_primary_10_1007_s11248_021_00240_3
crossref_primary_10_7717_peerj_17402
crossref_primary_10_18006_2024_12_4__537_556
crossref_primary_10_1007_s11248_021_00253_y
crossref_primary_10_1007_s11248_021_00238_x
crossref_primary_10_3389_fgeed_2021_663380
crossref_primary_10_1007_s00344_022_10760_9
crossref_primary_10_3390_plants12091892
crossref_primary_10_3389_fgene_2022_932859
crossref_primary_10_3389_fpls_2023_1121209
crossref_primary_10_1270_jsbbs_23049
crossref_primary_10_1002_fft2_70005
crossref_primary_10_1007_s42994_024_00195_z
crossref_primary_10_1016_j_copbio_2022_102856
crossref_primary_10_1093_jxb_erac352
crossref_primary_10_1007_s11033_023_09086_w
crossref_primary_10_1038_s41580_025_00834_3
crossref_primary_10_1007_s00425_022_03894_3
crossref_primary_10_3389_fgene_2022_1037091
crossref_primary_10_3389_fpls_2023_1122926
crossref_primary_10_3390_app122111275
crossref_primary_10_1016_j_biotechadv_2024_108382
crossref_primary_10_3389_fpls_2020_584151
crossref_primary_10_3389_fpls_2024_1304381
crossref_primary_10_1111_pbi_13613
crossref_primary_10_3390_ijms25020760
crossref_primary_10_3390_ijms22168752
crossref_primary_10_1016_j_nbt_2021_12_002
crossref_primary_10_3389_fgeed_2023_1138843
crossref_primary_10_1007_s11033_023_08239_1
crossref_primary_10_34133_bdr_0001
crossref_primary_10_1134_S1021443722010137
crossref_primary_10_1016_j_molp_2020_11_002
crossref_primary_10_3390_ijms241511920
crossref_primary_10_1021_acsagscitech_1c00279
crossref_primary_10_1093_plphys_kiac037
crossref_primary_10_3390_plants13192768
crossref_primary_10_1038_s41598_024_55088_4
crossref_primary_10_9787_PBB_2022_10_3_186
crossref_primary_10_3390_ijms25052606
crossref_primary_10_3389_fgene_2022_859437
crossref_primary_10_1093_pcp_pcab034
crossref_primary_10_3390_biology10121255
crossref_primary_10_3390_ijms22084206
crossref_primary_10_1007_s00425_022_03906_2
crossref_primary_10_3389_fgene_2022_866121
crossref_primary_10_3390_plants12020305
crossref_primary_10_1007_s11032_024_01452_1
crossref_primary_10_3389_fpls_2023_1271368
crossref_primary_10_1007_s00344_022_10890_0
crossref_primary_10_1111_tpj_70099
crossref_primary_10_1016_j_sajb_2024_07_038
crossref_primary_10_3390_agronomy13082038
crossref_primary_10_1016_j_plgene_2022_100369
crossref_primary_10_1111_pbi_13916
crossref_primary_10_3389_fcell_2020_622103
crossref_primary_10_1016_j_jgg_2021_04_003
crossref_primary_10_1016_j_plantsci_2023_111746
crossref_primary_10_3390_cells11182902
crossref_primary_10_3389_fpls_2020_586027
crossref_primary_10_1007_s00425_023_04187_z
crossref_primary_10_3389_fgeed_2022_830178
crossref_primary_10_3389_fpls_2021_681367
crossref_primary_10_1007_s44307_024_00041_9
crossref_primary_10_1073_pnas_2004834117
crossref_primary_10_1016_j_scienta_2025_113957
crossref_primary_10_1089_crispr_2021_0045
crossref_primary_10_3389_fpls_2023_1111680
crossref_primary_10_3389_fgeed_2020_612137
crossref_primary_10_1186_s12870_022_03519_7
crossref_primary_10_3389_frsus_2024_1378712
crossref_primary_10_3389_fnut_2021_751512
crossref_primary_10_1111_tpj_16943
crossref_primary_10_1360_TB_2023_1138
crossref_primary_10_1007_s00299_020_02622_z
crossref_primary_10_3389_fpls_2021_722552
crossref_primary_10_3389_fpls_2023_1260102
crossref_primary_10_3389_fpls_2023_1133036
crossref_primary_10_1111_pbi_14188
crossref_primary_10_1007_s11627_021_10187_z
crossref_primary_10_1111_pbi_13490
crossref_primary_10_3390_antiox9121225
crossref_primary_10_1093_jxb_erad072
crossref_primary_10_1007_s42994_024_00147_7
crossref_primary_10_1111_pbi_13417
crossref_primary_10_1093_hr_uhae187
crossref_primary_10_1111_jipb_13063
crossref_primary_10_1111_ppl_13547
crossref_primary_10_1007_s00122_021_03874_3
crossref_primary_10_1111_pce_14861
crossref_primary_10_1016_j_plaphy_2024_108507
crossref_primary_10_3390_biology12111400
crossref_primary_10_1038_s44222_023_00115_8
crossref_primary_10_3390_antiox12112014
crossref_primary_10_1038_s41477_024_01786_w
Cites_doi 10.1104/pp.16.00569
10.1038/nbt.3659
10.1038/nrmicro3117
10.1104/pp.111.193110
10.1101/gad.12.24.3831
10.1016/j.cell.2014.05.010
10.1093/nar/21.22.5034
10.1073/pnas.93.10.5055
10.1111/tpj.13446
10.1111/pbi.12868
10.1038/nbt.4202
10.1021/sb4001504
10.1073/pnas.1202191109
10.1007/s00705-013-1675-x
10.3389/fpls.2016.01683
10.1104/pp.15.01663
10.1096/fj.11-188508
10.1186/s12915-019-0629-5
10.1002/bit.20695
10.1093/jxb/ery245
10.1038/nbt.2655
10.3389/fpls.2016.01045
10.1111/j.1365-313X.2011.04676.x
10.1016/j.dnarep.2005.05.004
10.1038/sj.onc.1204767
10.1002/bit.10483
10.1093/nar/9.20.5233
10.1105/tpc.113.119792
10.1093/nar/gkt780
10.1007/s002990050456
10.1016/j.virol.2016.03.014
10.1093/jxb/eri123
10.1111/pbi.13275
10.1006/viro.1996.8353
10.1111/tpj.13932
10.1038/nature26155
10.1038/nature07845
10.1371/journal.pgen.1003529
10.1016/0092-8674(83)90331-8
10.1016/j.virol.2014.01.024
10.1186/s13059-015-0796-9
10.1038/s41467-017-01836-2
10.1016/j.cell.2015.09.038
10.1186/1746-4811-9-39
10.1371/journal.pone.0016765
10.1007/s000180050433
10.1126/science.1225829
10.1016/j.mrfmmm.2004.12.011
10.1111/tpj.13782
10.1101/251082
10.1074/jbc.274.41.29453
10.1093/nar/gkr606
ContentType Journal Article
Copyright 2020 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2020 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd
– notice: 2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
DBID 24P
AAYXX
CITATION
NPM
7QO
8FD
8FE
8FG
8FH
ABJCF
ABUWG
AEUYN
AFKRA
AZQEC
BBNVY
BENPR
BGLVJ
BHPHI
CCPQU
DWQXO
FR3
GNUQQ
HCIFZ
L6V
LK8
M7P
M7S
P64
PHGZM
PHGZT
PIMPY
PKEHL
PQEST
PQGLB
PQQKQ
PQUKI
PTHSS
7X8
7S9
L.6
5PM
DOI 10.1111/pbi.13373
DatabaseName Wiley Online Library Open Access
CrossRef
PubMed
Biotechnology Research Abstracts
Technology Research Database
ProQuest SciTech Collection
ProQuest Technology Collection
ProQuest Natural Science Collection
Materials Science & Engineering Collection
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Technology Collection
Natural Science Collection
ProQuest One
ProQuest Central Korea
Engineering Research Database
ProQuest Central Student
SciTech Premium Collection
ProQuest Engineering Collection
Biological Sciences
Biological Science Database
Engineering Database
Biotechnology and BioEngineering Abstracts
ProQuest Central Premium
ProQuest One Academic (New)
ProQuest Publicly Available Content Database
ProQuest One Academic Middle East (New)
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
Engineering Collection
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
PubMed
Publicly Available Content Database
ProQuest Central Student
Technology Collection
Technology Research Database
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
ProQuest Engineering Collection
Biotechnology Research Abstracts
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest Central (New)
Engineering Collection
Engineering Database
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Technology Collection
Biological Science Database
ProQuest SciTech Collection
Biotechnology and BioEngineering Abstracts
ProQuest One Academic UKI Edition
Materials Science & Engineering Collection
Engineering Research Database
ProQuest One Academic
ProQuest One Academic (New)
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
DatabaseTitleList

Publicly Available Content Database
AGRICOLA
MEDLINE - Academic
PubMed
CrossRef
Database_xml – sequence: 1
  dbid: 24P
  name: Wiley Online Library Open Access
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: 8FG
  name: ProQuest Technology Collection
  url: https://search.proquest.com/technologycollection1
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Agriculture
DocumentTitleAlternate Advancement of plant HDR by multi‐replicons
EISSN 1467-7652
EndPage 2143
ExternalDocumentID PMC7540044
32176419
10_1111_pbi_13373
PBI13373
Genre article
Journal Article
GrantInformation_xml – fundername: Rural Development Administration (RDA), Korea
– fundername: Program for New Plant Breeding Techniques
  funderid: PJ01478401
– fundername: National Research Foundation of Korea
  funderid: NRF 2017R1A4A1015515
– fundername: Next‐Generation BioGreen 21 Program
  funderid: PJ01322601
– fundername: Next-Generation BioGreen 21 Program
  grantid: PJ01322601
– fundername: National Research Foundation of Korea
  grantid: NRF 2017R1A4A1015515
– fundername: Program for New Plant Breeding Techniques
  grantid: PJ01478401
– fundername: Next‐Generation BioGreen 21 Program
  grantid: PJ01322601
– fundername: ;
  grantid: NRF 2017R1A4A1015515
GroupedDBID ---
.3N
.GA
.Y3
05W
0R~
10A
123
1OC
24P
29O
31~
33P
4.4
50Y
50Z
51W
51X
52M
52N
52O
52P
52S
52T
52W
52X
53G
5HH
5LA
5VS
66C
702
7PT
8-0
8-1
8-3
8-4
8-5
8FE
8FG
8FH
8UM
930
A03
A8Z
AAEVG
AAHBH
AAHHS
AANHP
AAONW
AAZKR
ABCQN
ABDBF
ABEML
ABIJN
ABJCF
ABPVW
ACBWZ
ACCFJ
ACCMX
ACIWK
ACPRK
ACRPL
ACSCC
ACUHS
ACXQS
ACYXJ
ADBBV
ADIZJ
ADKYN
ADNMO
ADZMN
AEEZP
AEIMD
AENEX
AEQDE
AEUQT
AEUYN
AFBPY
AFEBI
AFKRA
AFRAH
AFZJQ
AIWBW
AJBDE
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AMBMR
ASPBG
ATUGU
AVUZU
AVWKF
AZBYB
AZFZN
BAFTC
BBNVY
BCNDV
BDRZF
BENPR
BFHJK
BGLVJ
BHPHI
BNHUX
BROTX
BRXPI
BY8
CAG
CCPQU
COF
CS3
D-E
D-F
DPXWK
DR2
DU5
EAD
EAP
EBD
EBS
ECGQY
EDH
EJD
EMK
EMOBN
EST
ESX
F00
F01
F04
F5P
FEDTE
G-S
G.N
GODZA
GROUPED_DOAJ
H.T
H.X
HCIFZ
HF~
HOLLA
HVGLF
HZ~
IAO
IEP
IGS
IHE
ITC
IX1
J0M
KQ8
L6V
LC2
LC3
LH4
LK8
LP6
LP7
LW6
M7P
M7S
MK4
ML0
N04
N05
N9A
NF~
O66
O9-
OIG
OK1
P2P
P2X
P4D
PIMPY
PROAC
PTHSS
Q.N
Q11
QB0
QM4
QO4
R.K
ROL
RPM
RX1
SUPJJ
SV3
TUS
UB1
W8V
W99
WIH
WIN
WQJ
WRC
XG1
~IA
~KM
~WT
AAYXX
AGQPQ
CITATION
PHGZM
PHGZT
AAMMB
AEFGJ
AGXDD
AIDQK
AIDYY
NPM
PQGLB
7QO
8FD
ABUWG
AZQEC
DWQXO
FR3
GNUQQ
P64
PKEHL
PQEST
PQQKQ
PQUKI
7X8
7S9
L.6
5PM
ID FETCH-LOGICAL-c5423-a353c8bb3adbd63aa664eb3de319c0b141bb0e0878cca699b2f7435a2b5b00cd3
IEDL.DBID DR2
ISSN 1467-7644
1467-7652
IngestDate Thu Aug 21 18:16:35 EDT 2025
Fri Jul 11 18:31:25 EDT 2025
Fri Jul 11 03:28:49 EDT 2025
Wed Aug 13 04:37:16 EDT 2025
Mon Jul 21 06:00:56 EDT 2025
Thu Apr 24 23:05:59 EDT 2025
Tue Jul 01 02:34:45 EDT 2025
Wed Jan 22 16:32:09 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 10
Keywords CRISPR/Cpf1
gene targeting
genome editing
multi-replicon
CRISPR/Cas9
homology-directed repair
Language English
License Attribution
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c5423-a353c8bb3adbd63aa664eb3de319c0b141bb0e0878cca699b2f7435a2b5b00cd3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0002-1180-6232
OpenAccessLink https://proxy.k.utb.cz/login?url=https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.13373
PMID 32176419
PQID 2441294040
PQPubID 1096352
PageCount 11
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_7540044
proquest_miscellaneous_2524329574
proquest_miscellaneous_2377684941
proquest_journals_2441294040
pubmed_primary_32176419
crossref_citationtrail_10_1111_pbi_13373
crossref_primary_10_1111_pbi_13373
wiley_primary_10_1111_pbi_13373_PBI13373
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate October 2020
PublicationDateYYYYMMDD 2020-10-01
PublicationDate_xml – month: 10
  year: 2020
  text: October 2020
PublicationDecade 2020
PublicationPlace England
PublicationPlace_xml – name: England
– name: Southampton
– name: Hoboken
PublicationTitle Plant biotechnology journal
PublicationTitleAlternate Plant Biotechnol J
PublicationYear 2020
Publisher John Wiley & Sons, Inc
John Wiley and Sons Inc
Publisher_xml – name: John Wiley & Sons, Inc
– name: John Wiley and Sons Inc
References 2017; 8
2014; 452–453
2005; 572
1993; 21
2017; 89
2019; 17
2014; 26
2013; 9
2016; 34
1998; 17
1997; 227
2014; 3
2013; 11
1999; 56
2013; 158
2011; 68
2012; 26
2012; 337
1998; 12
2018; 36
2015; 163
2006; 93
2015; 16
2003; 81
2013; 41
1996; 93
1981; 9
2011; 39
2009; 459
2011; 6
2012; 109
2001; 20
2018; 69
1983; 33
2014; 157
2016; 7
2018; 556
2013; 31
1999; 274
2019
2005; 4
2018; 95
2018; 93
2012; 158
2016; 171
2016; 170
2018; 16
2005; 56
2016; 493
e_1_2_7_5_1
e_1_2_7_3_1
e_1_2_7_9_1
e_1_2_7_7_1
e_1_2_7_19_1
e_1_2_7_17_1
e_1_2_7_15_1
e_1_2_7_41_1
e_1_2_7_13_1
e_1_2_7_43_1
e_1_2_7_11_1
e_1_2_7_45_1
e_1_2_7_47_1
e_1_2_7_26_1
e_1_2_7_49_1
e_1_2_7_28_1
e_1_2_7_50_1
e_1_2_7_25_1
e_1_2_7_31_1
e_1_2_7_52_1
e_1_2_7_23_1
e_1_2_7_33_1
e_1_2_7_21_1
e_1_2_7_35_1
e_1_2_7_37_1
e_1_2_7_39_1
e_1_2_7_6_1
e_1_2_7_4_1
e_1_2_7_8_1
e_1_2_7_18_1
e_1_2_7_16_1
e_1_2_7_40_1
e_1_2_7_2_1
e_1_2_7_14_1
e_1_2_7_42_1
e_1_2_7_12_1
e_1_2_7_44_1
e_1_2_7_10_1
e_1_2_7_46_1
e_1_2_7_48_1
e_1_2_7_27_1
e_1_2_7_29_1
e_1_2_7_51_1
e_1_2_7_30_1
e_1_2_7_53_1
e_1_2_7_24_1
e_1_2_7_32_1
e_1_2_7_22_1
e_1_2_7_34_1
e_1_2_7_20_1
e_1_2_7_36_1
e_1_2_7_38_1
References_xml – volume: 39
  start-page: 9275
  year: 2011
  end-page: 9282
  article-title: The CRISPR/Cas system provides immunity in
  publication-title: Nucleic Acids Res.
– volume: 11
  start-page: 777
  year: 2013
  end-page: 788
  article-title: Geminiviruses: masters at redirecting and reprogramming plant processes
  publication-title: Nat. Rev. Microbiol.
– volume: 8
  start-page: 2024
  year: 2017
  article-title: CRISPR‐Cpf1 mediates efficient homology‐directed repair and temperature‐controlled genome editing
  publication-title: Nat. Commun.
– volume: 95
  start-page: 5
  year: 2018
  end-page: 16
  article-title: Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system
  publication-title: Plant J.
– volume: 171
  start-page: 2112
  year: 2016
  end-page: 2126
  article-title: A single amino‐acid substitution in the sodium transporter HKT1 associated with plant salt tolerance
  publication-title: Plant Physiol.
– start-page: 251082
  year: 2019
– volume: 9
  start-page: 5233
  year: 1981
  end-page: 5252
  article-title: Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes
  publication-title: Nucleic Acids Res.
– year: 2019
  article-title: Engineering CRISPR/LbCas12a for highly efficient, temperature‐tolerant plant gene editing
  publication-title: Plant Biotechnol. J
– volume: 163
  start-page: 759
  year: 2015
  end-page: 771
  article-title: Cpf1 is a single RNA‐guided endonuclease of a class 2 CRISPR‐Cas system
  publication-title: Cell
– volume: 31
  start-page: 691
  year: 2013
  end-page: 693
  article-title: Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA‐guided endonuclease
  publication-title: Nat. Biotechnol.
– volume: 93
  start-page: 271
  year: 2006
  end-page: 279
  article-title: Bean Yellow Dwarf Virus replicons for high‐level transgene expression in transgenic plants and cell cultures
  publication-title: Biotechnol. Bioeng.
– volume: 6
  year: 2011
  article-title: A modular cloning system for standardized assembly of multigene constructs
  publication-title: PLoS ONE
– volume: 337
  start-page: 816
  year: 2012
  end-page: 821
  article-title: A programmable dual‐RNA‐guided DNA endonuclease in adaptive bacterial immunity
  publication-title: Science
– volume: 4
  start-page: 1038
  year: 2005
  end-page: 1046
  article-title: Chromosomal aberrations induced by double strand DNA breaks
  publication-title: DNA Repair (Amst)
– volume: 41
  year: 2013
  article-title: Demonstration of CRISPR/Cas9/sgRNA‐mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice
  publication-title: Nucleic Acids Res.
– volume: 556
  start-page: 57
  year: 2018
  end-page: 63
  article-title: Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
  publication-title: Nature
– volume: 33
  start-page: 25
  year: 1983
  end-page: 35
  article-title: The double‐strand‐break repair model for recombination
  publication-title: Cell
– volume: 56
  start-page: 313
  year: 1999
  end-page: 329
  article-title: Geminivirus DNA replication
  publication-title: Cell. Mol. Life Sci.
– volume: 56
  start-page: 1
  year: 2005
  end-page: 14
  article-title: The repair of double‐strand breaks in plants: mechanisms and consequences for genome evolution
  publication-title: J. Exp. Bot.
– volume: 493
  start-page: 113
  year: 2016
  end-page: 127
  article-title: The recombination mediator RAD51D promotes geminiviral infection
  publication-title: Virology
– volume: 227
  start-page: 389
  year: 1997
  end-page: 399
  article-title: DNA replication of wheat dwarf geminivirus vectors: effects of origin structure and size
  publication-title: Virology
– volume: 3
  start-page: 839
  year: 2014
  end-page: 843
  article-title: A golden gate modular cloning toolbox for plants
  publication-title: ACS Synth. Biol.
– volume: 36
  start-page: 894
  year: 2018
  end-page: 898
  article-title: Genome editing of upstream open reading frames enables translational control in plants
  publication-title: Nat. Biotechnol.
– volume: 17
  start-page: 631
  year: 1998
  end-page: 639
  article-title: GUS expression patterns from a tobacco yellow dwarf virus‐based episomal vector
  publication-title: Plant Cell. Rep.
– volume: 81
  start-page: 430
  year: 2003
  end-page: 437
  article-title: Geminivirus vectors for high‐level expression of foreign proteins in plant cells
  publication-title: Biotechnol. Bioeng.
– volume: 20
  start-page: 5572
  year: 2001
  end-page: 5579
  article-title: DNA double strand break repair and chromosomal translocation: lessons from animal models
  publication-title: Oncogene
– volume: 109
  start-page: 7535
  year: 2012
  end-page: 7540
  article-title: In planta gene targeting
  publication-title: Proc. Natl Acad. Sci. USA
– volume: 16
  start-page: 232
  year: 2015
  article-title: High‐frequency, precise modification of the tomato genome
  publication-title: Genome Biol.
– volume: 9
  year: 2013
  article-title: Gene expression regulation by upstream open reading frames and human disease
  publication-title: PLoS Genet.
– volume: 21
  start-page: 5034
  year: 1993
  end-page: 5040
  article-title: Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site‐specific endonuclease
  publication-title: Nucleic Acids Res.
– volume: 93
  start-page: 377
  year: 2018
  end-page: 386
  article-title: Increased efficiency of targeted mutagenesis by CRISPR/Cas9 in plants using heat stress
  publication-title: Plant J.
– volume: 274
  start-page: 29453
  year: 1999
  end-page: 29462
  article-title: Yeast Rad54 promotes Rad51‐dependent homologous DNA pairing via ATP hydrolysis‐driven change in DNA double helix conformation
  publication-title: J. Biol. Chem.
– volume: 158
  start-page: 1931
  year: 2013
  end-page: 1941
  article-title: The host factor RAD51 is involved in mungbean yellow mosaic India virus (MYMIV) DNA replication
  publication-title: Arch. Virol.
– volume: 17
  start-page: 9
  issue: 1
  year: 2019
  article-title: Application of CRISPRCas12a temperature sensitivity for improved genome editing in rice, maize, and Arabidopsis
  publication-title: BMC Biol
– volume: 26
  start-page: 1142
  year: 2012
  end-page: 1160
  article-title: A novel role for RAD54: this host protein modulates geminiviral DNA replication
  publication-title: FASEB J.
– volume: 158
  start-page: 1463
  year: 2012
  end-page: 1474
  article-title: TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative , shows K(+) specificity in the presence of NaCl
  publication-title: Plant Physiol.
– volume: 68
  start-page: 159
  year: 2011
  end-page: 167
  article-title: Intron splicing suppresses RNA silencing in Arabidopsis
  publication-title: Plant J.
– volume: 26
  start-page: 151
  year: 2014
  end-page: 163
  article-title: DNA replicons for plant genome engineering
  publication-title: Plant Cell
– volume: 69
  start-page: 4715
  year: 2018
  end-page: 4721
  article-title: Synthesis‐dependent repair of Cpf1‐induced double strand DNA breaks enables targeted gene replacement in rice
  publication-title: J. Exp. Bot.
– volume: 170
  start-page: 667
  year: 2016
  end-page: 677
  article-title: Biallelic gene targeting in rice
  publication-title: Plant Physiol.
– volume: 7
  start-page: 1045
  year: 2016
  article-title: Geminivirus‐mediated genome editing in potato ( L.) using sequence‐specific nucleases
  publication-title: Front. Plant Sci.
– volume: 16
  start-page: 1275
  year: 2018
  end-page: 1282
  article-title: Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava
  publication-title: Plant Biotechnol. J.
– volume: 34
  start-page: 933
  year: 2016
  end-page: 941
  article-title: Applications of CRISPR technologies in research and beyond
  publication-title: Nat. Biotechnol.
– volume: 452–453
  start-page: 287
  year: 2014
  end-page: 296
  article-title: Somatic homologous recombination in plants is promoted by a geminivirus in a tissue‐selective manner
  publication-title: Virology
– volume: 572
  start-page: 73
  year: 2005
  end-page: 83
  article-title: Homologous recombination in plants is temperature and day‐length dependent
  publication-title: Mutat. Res.
– volume: 7
  start-page: 1683
  year: 2016
  article-title: Rapid evolution of manifold CRISPR systems for plant genome editing
  publication-title: Front. Plant Sci.
– volume: 459
  start-page: 442
  year: 2009
  end-page: 445
  article-title: High‐frequency modification of plant genes using engineered zinc‐finger nucleases
  publication-title: Nature
– volume: 89
  start-page: 1251
  year: 2017
  end-page: 1262
  article-title: High‐efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9
  publication-title: Plant J
– volume: 157
  start-page: 1262
  year: 2014
  end-page: 1278
  article-title: Development and applications of CRISPR‐Cas9 for genome engineering
  publication-title: Cell
– volume: 12
  start-page: 3831
  year: 1998
  end-page: 3842
  article-title: Double‐strand break repair by interchromosomal recombination: suppression of chromosomal translocations
  publication-title: Genes Dev.
– volume: 9
  start-page: 39
  year: 2013
  article-title: Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system
  publication-title: Plant Methods
– volume: 93
  start-page: 5055
  year: 1996
  end-page: 5060
  article-title: Two different but related mechanisms are used in plants for the repair of genomic double‐strand breaks by homologous recombination
  publication-title: Proc. Natl Acad. Sci. USA
– ident: e_1_2_7_3_1
  doi: 10.1104/pp.16.00569
– ident: e_1_2_7_6_1
  doi: 10.1038/nbt.3659
– ident: e_1_2_7_19_1
  doi: 10.1038/nrmicro3117
– ident: e_1_2_7_2_1
  doi: 10.1104/pp.111.193110
– ident: e_1_2_7_40_1
  doi: 10.1101/gad.12.24.3831
– ident: e_1_2_7_21_1
  doi: 10.1016/j.cell.2014.05.010
– ident: e_1_2_7_38_1
  doi: 10.1093/nar/21.22.5034
– ident: e_1_2_7_39_1
  doi: 10.1073/pnas.93.10.5055
– ident: e_1_2_7_17_1
  doi: 10.1111/tpj.13446
– ident: e_1_2_7_23_1
  doi: 10.1111/pbi.12868
– ident: e_1_2_7_53_1
  doi: 10.1038/nbt.4202
– ident: e_1_2_7_14_1
  doi: 10.1021/sb4001504
– ident: e_1_2_7_15_1
  doi: 10.1073/pnas.1202191109
– ident: e_1_2_7_46_1
  doi: 10.1007/s00705-013-1675-x
– ident: e_1_2_7_30_1
  doi: 10.3389/fpls.2016.01683
– ident: e_1_2_7_13_1
  doi: 10.1104/pp.15.01663
– ident: e_1_2_7_26_1
  doi: 10.1096/fj.11-188508
– ident: e_1_2_7_31_1
  doi: 10.1186/s12915-019-0629-5
– ident: e_1_2_7_52_1
  doi: 10.1002/bit.20695
– ident: e_1_2_7_29_1
  doi: 10.1093/jxb/ery245
– ident: e_1_2_7_35_1
  doi: 10.1038/nbt.2655
– ident: e_1_2_7_9_1
  doi: 10.3389/fpls.2016.01045
– ident: e_1_2_7_11_1
  doi: 10.1111/j.1365-313X.2011.04676.x
– ident: e_1_2_7_49_1
  doi: 10.1016/j.dnarep.2005.05.004
– ident: e_1_2_7_16_1
  doi: 10.1038/sj.onc.1204767
– ident: e_1_2_7_32_1
  doi: 10.1002/bit.10483
– ident: e_1_2_7_27_1
  doi: 10.1093/nar/9.20.5233
– ident: e_1_2_7_4_1
  doi: 10.1105/tpc.113.119792
– ident: e_1_2_7_24_1
  doi: 10.1093/nar/gkt780
– ident: e_1_2_7_34_1
  doi: 10.1007/s002990050456
– ident: e_1_2_7_42_1
  doi: 10.1016/j.virol.2016.03.014
– ident: e_1_2_7_37_1
  doi: 10.1093/jxb/eri123
– ident: e_1_2_7_44_1
  doi: 10.1111/pbi.13275
– ident: e_1_2_7_45_1
  doi: 10.1006/viro.1996.8353
– ident: e_1_2_7_12_1
  doi: 10.1111/tpj.13932
– ident: e_1_2_7_22_1
  doi: 10.1038/nature26155
– ident: e_1_2_7_48_1
  doi: 10.1038/nature07845
– ident: e_1_2_7_5_1
  doi: 10.1371/journal.pgen.1003529
– ident: e_1_2_7_47_1
  doi: 10.1016/0092-8674(83)90331-8
– ident: e_1_2_7_41_1
  doi: 10.1016/j.virol.2014.01.024
– ident: e_1_2_7_10_1
  doi: 10.1186/s13059-015-0796-9
– ident: e_1_2_7_33_1
  doi: 10.1038/s41467-017-01836-2
– ident: e_1_2_7_51_1
  doi: 10.1016/j.cell.2015.09.038
– ident: e_1_2_7_7_1
  doi: 10.1186/1746-4811-9-39
– ident: e_1_2_7_50_1
  doi: 10.1371/journal.pone.0016765
– ident: e_1_2_7_18_1
  doi: 10.1007/s000180050433
– ident: e_1_2_7_25_1
  doi: 10.1126/science.1225829
– ident: e_1_2_7_8_1
  doi: 10.1016/j.mrfmmm.2004.12.011
– ident: e_1_2_7_28_1
  doi: 10.1111/tpj.13782
– ident: e_1_2_7_20_1
  doi: 10.1101/251082
– ident: e_1_2_7_36_1
  doi: 10.1074/jbc.274.41.29453
– ident: e_1_2_7_43_1
  doi: 10.1093/nar/gkr606
SSID ssj0021656
Score 2.5921247
Snippet Summary Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by...
Genome editing via the homology‐directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error‐prone repair by nonhomologous end...
Genome editing via the homology-directed repair (HDR) pathway in somatic plant cells is very inefficient compared with error-prone repair by nonhomologous end...
SourceID pubmedcentral
proquest
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 2133
SubjectTerms Alleles
Antibiotics
Binding sites
biotechnology
Cell culture
Cloning
CRISPR
CRISPR/Cas9
CRISPR/Cpf1
Deoxyribonucleic acid
DNA
Editing
Efficiency
gene targeting
Genetic transformation
genome editing
Genomes
genomics
Germination
Heredity
Homology
homology‐directed repair
multi‐replicon
Mutation
Non-homologous end joining
Offspring
phenotypic selection
Plant cells
progeny
Proteins
Repair
replicon
Reproduction (biology)
salt tolerance
self-pollination
Sodium chloride
temperature
Tomatoes
SummonAdditionalLinks – databaseName: ProQuest Central
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1LT9wwEB61cGkPqG_S0spUHLikJPErPiFYgYADWm1B4tQojp1lpSXZLsuht_6E_sb-EsaON-2Kllskj0aJ521PvgHYyU0tc6NMzA2vY6a5iLWq0RlKVteMJpp3DbLn4uSSnV3xq3DgdhvaKpc-0Ttq01bujHwPwxCGJoY6tz_7HrupUe52NYzQeArr6IJzLL7WD4_Oh6O-5HLYMt3_RTKWGPoDtpDr5ZnpyRcs0CRdjUgP0syH3ZJ_Z7E-DB2_gI2QP5KDTuAv4YltXsHzg_E8YGjY1_DN9W5MfxDr0SGQHblub_zp-e-fv7oQZg2ZYxyazInrex-Twej063C0N5jVKdKMPeCI6_6dOrIpKktDJg1ZtJjetm_g8vjoYnAShzEKccUxWYpLymmVa01Lo42gZSkEwxLaWLS-KtEpS7VObJLLHKUplNJZjWkFLzPN0SYrQ9_CWtM2dhOITbPaCuXYMWTNcpXZRFRUGMaZSMoIdpdbWVQBY9yNupgWy1oDd73wux7B55501gFr_ItoaymPItjWbfFHEyLY7pfRKtxVR9nY9g5pqHQ3jIqlj9DwjNFMcckieNeJuH8TipWaYKmKQK4IvydwqNyrK83k2qNzS-7cIvLc9Wry_48rhoen_uH941_5AZ5lrsj3HYRbsLaY39mPmAkt9Keg7vch4Qr2
  priority: 102
  providerName: ProQuest
Title Highly efficient homology‐directed repair using CRISPR/Cpf1‐geminiviral replicon in tomato
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.13373
https://www.ncbi.nlm.nih.gov/pubmed/32176419
https://www.proquest.com/docview/2441294040
https://www.proquest.com/docview/2377684941
https://www.proquest.com/docview/2524329574
https://pubmed.ncbi.nlm.nih.gov/PMC7540044
Volume 18
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9NAEB6V9gKH8qYuJTKIQy8OtvflFac2atpyqKJApR4Qlte7TiNSO0qTA5z4CfxGfgmz64caCghxsSx5vNq1Z3a-2f38GeB1oguRaKkDplkRUMV4oGSBk6GgRUFJqFhNkD3jJ-f03QW72IC37bcwtT5Et-BmI8PN1zbAM3V9I8jnatrHAktYpU_L1bKAaNxJR8VWVab-skgEApN-oypkWTzdneu56BbAvM2TvIlfXQIa3oePbddr3snn_mqp-vnXX1Qd_3NsD2C7Aab-Qe1JD2HDlI_g3sFk0YhzmMfwyZJCZl9842QnsLf-ZXXlluV_fPte50aj_QUmuOnCt4T6iT8Yn74fjd8M5kWENhOnZGJpxTNrNkMvLP1p6S8rxM3VEzgfHn0YnATN_xmCnCEKCzLCSJ4oRTKtNCdZxjnF2lwbDOs8VBGNlApNmIgE3YRLqeIC8QrLYsUw2HNNnsJmWZVmB3wTxYXh0jZHsWmayNiEPCdcU0Z5mHmw376pNG_Ey-0_NGZpW8TgI0vdI_PgVWc6rxU7fme0177utAna6xSRDqIfitOaBy-7yxhudg8lK021Qhsi7NalpNFfbFhMSSyZoB48qz2o6wnBEpDTSHog1nyrM7By3-tXyumlk_0WzM632Oa-c50_Dy4dHZ66k91_N30Od2O7kuBoinuwuVyszAuEW0vVgzsxHeExGR73YOvw6Gw07rmli56LuJ9RMS30
linkProvider Wiley-Blackwell
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3NbtQwEB6VcgAOiP8GChgEUi9pk_gvOSBUFpZdWqqqtFJPpHHsbFdakmW7FeqNR-BJeCiehLHzA6tCb71F8mgUez57ZuzxZ4AXsS5krBPtc80LnykufJUUuBhKVhSMBorXBbI7YnDAPhzywyX42d6FsWWV7ZroFmpd5XaPfAPdELomhph7Pf3q21ej7Olq-4RGDYstc_YNU7aTV8O3aN-XUdR_t98b-M2rAn7OMXbwM8ppHitFM620oFkmBMOMUhsEYx6okIVKBSaIZYydE0miogK9LM8ixRGiuaao9wpcZZQmdkbF_fddgmeZbOrbTNKXGGg0TEa2cmiqxuuYDkq66P_OBbXnazP_jpmd0-vfgptNtEo2a3jdhiVT3oEbm6NZw9hh7sJnWykyOSPGcVGgOnJcfXF79b--_6gdptFkhl5vPCO2yn5EenvDT7t7G71pEaLMyNGb2FrjiRWbIDRLMi7JvMJguroHB5cyvPdhuaxKswLEhFFhRGLVMVTN4iQygcip0IwzEWQerLVDmeYNo7l9WGOStpkNjnrqRt2D553otKbx-JfQamuPtJnJJ-kf3HnwrGvGOWgPVrLSVKcoQ6U9z0xYeIEMjxiNEi6ZBw9qE3d_QjEvFCxMPJALxu8ELAf4Yks5PnZc4JLbRRh1rjmY_L9z6e6boft4eHEvn8K1wf7H7XR7uLP1CK5HdnvB1S6uwvJ8dmoeYww2V08c8AkcXfZM-w0QVEdK
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3NbtNAEB6VVEL0gPjHUMAgkHoxsb1_9gGhNm3UUBRFgUo91Xi96zRSaoc0FeqNR-B5eByehNn1D0SF3nqz5NHIu_vtzszu528BXkcqF5GKlccUyz0qGfdknONiKGieU-JLVhFkh3z_kH44Ykdr8LP5F8bQKps10S7UqszMHnkXwxCGJoqY6-Y1LWK0238__-qZG6TMSWtznUYFkQN98Q3Lt7N3g10c6zdh2N_73Nv36hsGvIxhHuGlhJEskpKkSipO0pRzitWl0gjMzJcBDaT0tR-JCBvK41iGOUZcloaSIVwzRdDvDVgXWBX5HVjf2RuOxm25Z3Rtqn-bhCcw7ah1jQyPaC6nb7E4FGQ1Gl5KcS8zNf_OoG0I7N-B23Xu6m5XYLsLa7q4Bxvbk0Wt36Hvw7HhjcwuXG2VKdCde1Ke2p37X99_VOFTK3eBMXC6cA3nfuL2xoNPo3G3N88DtJlYsRPDPJ4ZsxkCtXCnhbssMbUuH8DhtXTwQ-gUZaEfg6uDMNc8Nu4ouqZRHGqfZ4Qryij3Uwe2mq5Mslrf3FyzMUuaOgd7PbG97sCr1nReiXr8y2izGY-kntdnyR8UOvCyfY0z0hyzpIUuz9GGCHO6GdPgChsWUhLGTFAHHlVD3H4JwSqR0yB2QKwMfmtgFMFX3xTTE6sMLphZktHnloXJ_xuXjHYG9uHJ1a18ATdxliUfB8ODp3ArNHsNlsi4CZ3l4lw_w4RsKZ_XyHfhy3VPtt-H2Uzc
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Highly+efficient+homology%E2%80%90directed+repair+using+CRISPR%2FCpf1%E2%80%90geminiviral+replicon+in+tomato&rft.jtitle=Plant+biotechnology+journal&rft.au=Vu%2C+Tien+Van&rft.au=Sivankalyani%2C+Velu&rft.au=Kim%2C+Eun%E2%80%90Jung&rft.au=Doan%2C+Duong+Thi+Hai&rft.date=2020-10-01&rft.pub=John+Wiley+and+Sons+Inc&rft.issn=1467-7644&rft.eissn=1467-7652&rft.volume=18&rft.issue=10&rft.spage=2133&rft.epage=2143&rft_id=info:doi/10.1111%2Fpbi.13373&rft_id=info%3Apmid%2F32176419&rft.externalDocID=PMC7540044
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1467-7644&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1467-7644&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1467-7644&client=summon