Reduced fire blight susceptibility in apple cultivars using a high‐efficiency CRISPR/Cas9‐FLP/FRT‐based gene editing system

Summary The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars...

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Published inPlant biotechnology journal Vol. 18; no. 3; pp. 845 - 858
Main Authors Pompili, Valerio, Dalla Costa, Lorenza, Piazza, Stefano, Pindo, Massimo, Malnoy, Mickael
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.03.2020
John Wiley and Sons Inc
Subjects
Agrobacterium radiobacter
Agrobacterium tumefaciens
Apple
Apples
bacteria
biotechnology
Blight
Cassettes
Cloning
Comparative analysis
CRISPR
CRISPR-Cas systems
Crop diseases
Cultivars
Deoxyribonucleic acid
DIPM
DNA
DNA sequencing
Efficiency
Erwinia amylovora
fire blight
FLP/FRT recombination
FRT gene
Fruits
gene editing
Gene expression
Genes
genetic markers
Genetic modification
Genetically altered foods
genetically modified organisms
Genomes
Health aspects
heat treatment
Kinases
loss-of-function mutation
Malus domestica
Malus × domestica
Mutation
Neomycin
Pathogens
Proteins
quantitative polymerase chain reaction
Recombination
Signal transduction
Malus × domestica
DIPM
fire blight
gene editing
FLP/FRT recombination
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Abstract Summary The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty‐seven transgenic lines were screened to identify CRISPR/Cas9‐induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss‐of‐function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off‐target sites revealed no mutation event. Moreover, our construct contained a heat‐shock inducible FLP/FRT recombination system designed specifically to remove the T‐DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat‐treated and screened by real‐time PCR to quantify the exogenous DNA elimination. The T‐DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9‐FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.
AbstractList The bacterium Erwinia amylovora , the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein Md DIPM 4. In this work, Md DIPM 4 knockout has been produced in two Malus  ×  domestica susceptible cultivars using the CRISPR /Cas9 system delivered via Agrobacterium tumefaciens . Fifty‐seven transgenic lines were screened to identify CRISPR /Cas9‐induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss‐of‐function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off‐target sites revealed no mutation event. Moreover, our construct contained a heat‐shock inducible FLP / FRT recombination system designed specifically to remove the T‐ DNA harbouring the expression cassettes for CRISPR /Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat‐treated and screened by real‐time PCR to quantify the exogenous DNA elimination. The T‐ DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR /Cas9‐ FLP / FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA .
Summary The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty‐seven transgenic lines were screened to identify CRISPR/Cas9‐induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss‐of‐function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off‐target sites revealed no mutation event. Moreover, our construct contained a heat‐shock inducible FLP/FRT recombination system designed specifically to remove the T‐DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat‐treated and screened by real‐time PCR to quantify the exogenous DNA elimination. The T‐DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9‐FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.
The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty-seven transgenic lines were screened to identify CRISPR/Cas9-induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss-of-function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off-target sites revealed no mutation event. Moreover, our construct contained a heat-shock inducible FLP/FRT recombination system designed specifically to remove the T-DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat-treated and screened by real-time PCR to quantify the exogenous DNA elimination. The T-DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9-FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty-seven transgenic lines were screened to identify CRISPR/Cas9-induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss-of-function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off-target sites revealed no mutation event. Moreover, our construct contained a heat-shock inducible FLP/FRT recombination system designed specifically to remove the T-DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat-treated and screened by real-time PCR to quantify the exogenous DNA elimination. The T-DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9-FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.
The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty‐seven transgenic lines were screened to identify CRISPR/Cas9‐induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss‐of‐function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off‐target sites revealed no mutation event. Moreover, our construct contained a heat‐shock inducible FLP/FRT recombination system designed specifically to remove the T‐DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat‐treated and screened by real‐time PCR to quantify the exogenous DNA elimination. The T‐DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9‐FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.
The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the apple susceptibility protein MdDIPM4. In this work, MdDIPM4 knockout has been produced in two Malus × domestica susceptible cultivars using the CRISPR/Cas9 system delivered via Agrobacterium tumefaciens. Fifty-seven transgenic lines were screened to identify CRISPR/Cas9-induced mutations. An editing efficiency of 75% was obtained. Seven edited lines with a loss-of-function mutation were inoculated with the pathogen. Highly significant reduction in susceptibility was observed compared to control plants. Sequencing of five potential off-target sites revealed no mutation event. Moreover, our construct contained a heat-shock inducible FLP/FRT recombination system designed specifically to remove the T-DNA harbouring the expression cassettes for CRISPR/Cas9, the marker gene and the FLP itself. Six plant lines with reduced susceptibility to the pathogen were heat-treated and screened by real-time PCR to quantify the exogenous DNA elimination. The T-DNA removal was further validated by sequencing in one plant line. To our knowledge, this work demonstrates for the first time the development and application of a CRISPR/Cas9-FLP/FRT gene editing system for the production of edited apple plants carrying a minimal trace of exogenous DNA.
Audience Academic
Author Dalla Costa, Lorenza
Pindo, Massimo
Piazza, Stefano
Pompili, Valerio
Malnoy, Mickael
AuthorAffiliation 1 Department of Genomics and Biology of Fruit Crops Research and Innovation Centre Fondazione Edmund Mach San Michele all'Adige Italy
2 Department of Agricultural, Food, Environmental and Animal Sciences Università degli Studi di Udine Udine Italy
AuthorAffiliation_xml – name: 2 Department of Agricultural, Food, Environmental and Animal Sciences Università degli Studi di Udine Udine Italy
– name: 1 Department of Genomics and Biology of Fruit Crops Research and Innovation Centre Fondazione Edmund Mach San Michele all'Adige Italy
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  givenname: Valerio
  orcidid: 0000-0003-1393-1245
  surname: Pompili
  fullname: Pompili, Valerio
  email: valerio.pompili@guests.fmach.it
  organization: Università degli Studi di Udine
– sequence: 2
  givenname: Lorenza
  surname: Dalla Costa
  fullname: Dalla Costa, Lorenza
  organization: Fondazione Edmund Mach
– sequence: 3
  givenname: Stefano
  surname: Piazza
  fullname: Piazza, Stefano
  organization: Fondazione Edmund Mach
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  surname: Pindo
  fullname: Pindo, Massimo
  organization: Fondazione Edmund Mach
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  givenname: Mickael
  surname: Malnoy
  fullname: Malnoy, Mickael
  email: mickael.malnoy@fmach.it
  organization: Fondazione Edmund Mach
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31495052$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2019 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
COPYRIGHT 2020 John Wiley & Sons, Inc.
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: 2019 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: COPYRIGHT 2020 John Wiley & Sons, Inc.
– 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.
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Issue 3
Keywords Malus × domestica
DIPM
fire blight
gene editing
FLP/FRT recombination
Language English
License Attribution
2019 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.
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  article-title: Stability of fire blight resistance in apple
  publication-title: Eucarpia Symp. Fruit Breed. Genet.
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Snippet Summary The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts...
The bacterium Erwinia amylovora , the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the...
The bacterium Erwinia amylovora, the causal agent of fire blight disease in apple, triggers its infection through the DspA/E effector which interacts with the...
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SubjectTerms Agrobacterium radiobacter
Agrobacterium tumefaciens
Apple
Apples
bacteria
biotechnology
Blight
Cassettes
Cloning
Comparative analysis
CRISPR
CRISPR-Cas systems
Crop diseases
Cultivars
Deoxyribonucleic acid
DIPM
DNA
DNA sequencing
Efficiency
Erwinia amylovora
fire blight
FLP/FRT recombination
FRT gene
Fruits
gene editing
Gene expression
Genes
genetic markers
Genetic modification
Genetically altered foods
genetically modified organisms
Genomes
Health aspects
heat treatment
Kinases
loss-of-function mutation
Malus domestica
Malus × domestica
Mutation
Neomycin
Pathogens
Proteins
quantitative polymerase chain reaction
Recombination
Signal transduction
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Title Reduced fire blight susceptibility in apple cultivars using a high‐efficiency CRISPR/Cas9‐FLP/FRT‐based gene editing system
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.13253
https://www.ncbi.nlm.nih.gov/pubmed/31495052
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Volume 18
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