A viral guide RNA delivery system for CRISPR-based transcriptional activation and heritable targeted DNA demethylation in Arabidopsis thaliana

Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has a...

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Published inPLoS genetics Vol. 16; no. 12; p. e1008983
Main Authors Ghoshal, Basudev, Vong, Brandon, Picard, Colette L., Feng, Suhua, Tam, Janet M., Jacobsen, Steven E.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 14.12.2020
Public Library of Science (PLoS)
Subjects
Arabidopsis
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biology and life sciences
CRISPR
CRISPR-Cas Systems
Demethylation
Deoxyribonucleic acid
Diseases and pests
Distribution
DNA
DNA Methylation
Drug delivery systems
Drugs
Engineering and Technology
Epigenetics
Epigenome
Experiments
Gene Editing - methods
Gene expression
Gene regulation
Gene Targeting - methods
Genetic aspects
Genomes
Innovations
Plant Viruses - genetics
Proteins
Repressors
Research and Analysis Methods
Ribonucleic acid
RNA
RNA, Guide, CRISPR-Cas Systems - genetics
RNA, Transfer - genetics
Tobacco mosaic virus
Transcription activation
Transcription factors
Transcriptional Activation
Transcriptional coactivators
Transgenic plants
Vectors (Biology)
Vehicles
Viruses
United States
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Abstract Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana . Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing.
AbstractList Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana. Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing.
Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana . Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing. The discovery of CRISPR-CAS9 and its non-catalytic variants have provided enormous capacity for crop improvement and basic research by modifying the genome and the epigenome. The standard methods for delivering genome and epigenome editing reagents to plants consist of generating stable transgenic lines through tissue culture processes, which have several drawbacks including the need for plant regeneration and crossing. To overcome some of these challenges, plant virus-based platforms are being developed for genome editing. Although viruses have a limited cargo capacity, limiting the use of viruses to encode entire editing systems, guide RNAs have been successfully delivered to transgenic CAS9 expressing plants for genome editing. However, the use of viruses for CRISPR-based epigenome editing and transcriptional activation have not yet been explored. In this study we show that viral delivery of guide RNAs using a modified tobacco rattle virus can be used for transcriptional activation and heritable epigenome editing. This study advances the use of plant RNA viruses as delivery agents for epigenome editing.
Introduction Tools that enable targeted regulation of gene expression provide powerful systems for studying and manipulating diverse cellular processes [1]. Targeted gene regulation at the transcriptional level can be achieved by recruiting transcriptional activators, repressors, or epigenetic modifiers to a particular genomic locus using a programmable DNA-binding module, such as the catalytically inactive version of the CRISPR-CAS9 system [1–3]. The limitation in cargo capacity means that viral delivery of the entire editing system remains challenging in plants. [...]the viral-based delivery systems currently available for CRISPR-CAS9 genome editing systems are mainly focused on the delivery of guide RNA component of the system. [...]viral delivery of guide RNAs to transgenic CAS9 plants may provide the advantage of bypassing the repeated need to generate transgenic plants expressing different guide RNAs each time a new gene is targeted.
Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana. Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing.Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana. Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing.
Introduction Tools that enable targeted regulation of gene expression provide powerful systems for studying and manipulating diverse cellular processes [1]. Targeted gene regulation at the transcriptional level can be achieved by recruiting transcriptional activators, repressors, or epigenetic modifiers to a particular genomic locus using a programmable DNA-binding module, such as the catalytically inactive version of the CRISPR-CAS9 system [1–3]. The limitation in cargo capacity means that viral delivery of the entire editing system remains challenging in plants. [...]the viral-based delivery systems currently available for CRISPR-CAS9 genome editing systems are mainly focused on the delivery of guide RNA component of the system. [...]viral delivery of guide RNAs to transgenic CAS9 plants may provide the advantage of bypassing the repeated need to generate transgenic plants expressing different guide RNAs each time a new gene is targeted.
Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing this concept, several viral-based guide RNA delivery platforms for CRISPR-Cas9 genome editing have been developed. The CRISPR-Cas9 system has also been adapted for epigenome editing. While systems have been developed for CRISPR-Cas9 based gene activation or site-specific DNA demethylation, viral delivery of guide RNAs remains to be developed for these purposes. To address this gap we have developed a tobacco rattle virus (TRV)-based single guide RNA delivery system for epigenome editing in Arabidopsis thaliana . Because tRNA-like sequences have been shown to facilitate the cell-to-cell movement of RNAs in plants, we used the tRNA-guide RNA expression system to express guide RNAs from the viral genome to promote heritable epigenome editing. We demonstrate that the tRNA-gRNA system with TRV can be used for both transcriptional activation and targeted DNA demethylation of the FLOWERING WAGENINGEN gene in Arabidopsis. We achieved up to ~8% heritability of the induced demethylation phenotype in the progeny of virus inoculated plants. We did not detect the virus in the next generation, indicating effective clearance of the virus from plant tissues. Thus, TRV delivery, combined with a specific tRNA-gRNA architecture, provides for fast and effective epigenome editing.
Audience Academic
Author Ghoshal, Basudev
Vong, Brandon
Picard, Colette L.
Jacobsen, Steven E.
Feng, Suhua
Tam, Janet M.
AuthorAffiliation 1 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, California, United States of America
2 Eli and Edyth Broad Center of Regenerative Medicine and Stem Cell Research, University of California at Los Angeles, Los Angeles, California, United States of America
3 Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, California, United States of America
University of Minnesota, UNITED STATES
AuthorAffiliation_xml – name: 3 Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, California, United States of America
– name: 1 Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, California, United States of America
– name: 2 Eli and Edyth Broad Center of Regenerative Medicine and Stem Cell Research, University of California at Los Angeles, Los Angeles, California, United States of America
– name: University of Minnesota, UNITED STATES
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33315895$$D View this record in MEDLINE/PubMed
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Snippet Plant RNA viruses are used as delivery vectors for their high level of accumulation and efficient spread during virus multiplication and movement. Utilizing...
Introduction Tools that enable targeted regulation of gene expression provide powerful systems for studying and manipulating diverse cellular processes [1]....
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SubjectTerms Arabidopsis
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biology and life sciences
CRISPR
CRISPR-Cas Systems
Demethylation
Deoxyribonucleic acid
Diseases and pests
Distribution
DNA
DNA Methylation
Drug delivery systems
Drugs
Engineering and Technology
Epigenetics
Epigenome
Experiments
Gene Editing - methods
Gene expression
Gene regulation
Gene Targeting - methods
Genetic aspects
Genomes
Innovations
Plant Viruses - genetics
Proteins
Repressors
Research and Analysis Methods
Ribonucleic acid
RNA
RNA, Guide, CRISPR-Cas Systems - genetics
RNA, Transfer - genetics
Tobacco mosaic virus
Transcription activation
Transcription factors
Transcriptional Activation
Transcriptional coactivators
Transgenic plants
Vectors (Biology)
Vehicles
Viruses
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Title A viral guide RNA delivery system for CRISPR-based transcriptional activation and heritable targeted DNA demethylation in Arabidopsis thaliana
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Volume 16
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