One-pot Golden Gate Assembly of an avian infectious bronchitis virus reverse genetics system

Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapi...

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Published inPloS one Vol. 19; no. 7; p. e0307655
Main Authors Bilotti, Katharina, Keep, Sarah, Sikkema, Andrew P., Pryor, John M., Kirk, James, Foldes, Katalin, Doyle, Nicole, Wu, Ge, Freimanis, Graham, Dowgier, Giulia, Adeyemi, Oluwapelumi, Tabatabaei, S. Kasra, Lohman, Gregory J. S., Bickerton, Erica
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 25.07.2024
Public Library of Science (PLoS)
Subjects
Animals
Artificial chromosomes
Assembly
Avian infectious bronchitis
Bacterial infections
Biology
Biology and Life Sciences
Breakpoints
Bronchitis
Coronavirus Infections - veterinary
Coronavirus Infections - virology
DNA
DNA damage
E coli
Escherichia coli
Escherichia coli - genetics
Food security
Food supply
Fragments
Genetics
Genome, Viral
Genomes
Genomic instability
Genomics
Immunization
Infections
Infectious bronchitis virus - genetics
Laboratories
Medicine and Health Sciences
Molecular biology
Mortality
Pathogens
Plasmids
Plasmids - genetics
Population genetics
Poultry
Poultry Diseases - virology
Research and Analysis Methods
Respiratory diseases
Reverse Genetics - methods
Severe acute respiratory syndrome coronavirus 2
Site fidelity
Vaccine development
Vaccines
Viruses
Zoonoses
United Kingdom
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0307655

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Abstract Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapid response to emerging variants. Classic methods of reverse genetics for IBV can be time consuming, rely on recombination for the introduction of mutations, and, depending on the system, can be subject to genome instability and unreliable success rates. In this study, we have applied data-optimized Golden Gate Assembly design to create a rapidly executable, flexible, and faithful reverse genetics system for IBV. The IBV genome was divided into 12 fragments at high-fidelity fusion site breakpoints. All fragments were synthetically produced and propagated in E . coli plasmids, amenable to standard molecular biology techniques for DNA manipulation. The assembly can be carried out in a single reaction, with the products used directly in subsequent viral rescue steps. We demonstrate the use of this system for generation of point mutants and gene replacements. This Golden Gate Assembly-based reverse genetics system will enable rapid response to emerging variants of IBV, particularly important to vaccine development for controlling spread within poultry populations.
AbstractList Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapid response to emerging variants. Classic methods of reverse genetics for IBV can be time consuming, rely on recombination for the introduction of mutations, and, depending on the system, can be subject to genome instability and unreliable success rates. In this study, we have applied data-optimized Golden Gate Assembly design to create a rapidly executable, flexible, and faithful reverse genetics system for IBV. The IBV genome was divided into 12 fragments at high-fidelity fusion site breakpoints. All fragments were synthetically produced and propagated in E . coli plasmids, amenable to standard molecular biology techniques for DNA manipulation. The assembly can be carried out in a single reaction, with the products used directly in subsequent viral rescue steps. We demonstrate the use of this system for generation of point mutants and gene replacements. This Golden Gate Assembly-based reverse genetics system will enable rapid response to emerging variants of IBV, particularly important to vaccine development for controlling spread within poultry populations.
Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapid response to emerging variants. Classic methods of reverse genetics for IBV can be time consuming, rely on recombination for the introduction of mutations, and, depending on the system, can be subject to genome instability and unreliable success rates. In this study, we have applied data-optimized Golden Gate Assembly design to create a rapidly executable, flexible, and faithful reverse genetics system for IBV. The IBV genome was divided into 12 fragments at high-fidelity fusion site breakpoints. All fragments were synthetically produced and propagated in E. coli plasmids, amenable to standard molecular biology techniques for DNA manipulation. The assembly can be carried out in a single reaction, with the products used directly in subsequent viral rescue steps. We demonstrate the use of this system for generation of point mutants and gene replacements. This Golden Gate Assembly-based reverse genetics system will enable rapid response to emerging variants of IBV, particularly important to vaccine development for controlling spread within poultry populations.
Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapid response to emerging variants. Classic methods of reverse genetics for IBV can be time consuming, rely on recombination for the introduction of mutations, and, depending on the system, can be subject to genome instability and unreliable success rates. In this study, we have applied data-optimized Golden Gate Assembly design to create a rapidly executable, flexible, and faithful reverse genetics system for IBV. The IBV genome was divided into 12 fragments at high-fidelity fusion site breakpoints. All fragments were synthetically produced and propagated in E. coli plasmids, amenable to standard molecular biology techniques for DNA manipulation. The assembly can be carried out in a single reaction, with the products used directly in subsequent viral rescue steps. We demonstrate the use of this system for generation of point mutants and gene replacements. This Golden Gate Assembly-based reverse genetics system will enable rapid response to emerging variants of IBV, particularly important to vaccine development for controlling spread within poultry populations.Avian infectious bronchitis is an acute respiratory disease of poultry of particular concern for global food security. Investigation of infectious bronchitis virus (IBV), the causative agent of avian infectious bronchitis, via reverse genetics enables deeper understanding of virus biology and a rapid response to emerging variants. Classic methods of reverse genetics for IBV can be time consuming, rely on recombination for the introduction of mutations, and, depending on the system, can be subject to genome instability and unreliable success rates. In this study, we have applied data-optimized Golden Gate Assembly design to create a rapidly executable, flexible, and faithful reverse genetics system for IBV. The IBV genome was divided into 12 fragments at high-fidelity fusion site breakpoints. All fragments were synthetically produced and propagated in E. coli plasmids, amenable to standard molecular biology techniques for DNA manipulation. The assembly can be carried out in a single reaction, with the products used directly in subsequent viral rescue steps. We demonstrate the use of this system for generation of point mutants and gene replacements. This Golden Gate Assembly-based reverse genetics system will enable rapid response to emerging variants of IBV, particularly important to vaccine development for controlling spread within poultry populations.
Audience Academic
Author Pryor, John M.
Sikkema, Andrew P.
Freimanis, Graham
Doyle, Nicole
Wu, Ge
Bilotti, Katharina
Lohman, Gregory J. S.
Foldes, Katalin
Tabatabaei, S. Kasra
Dowgier, Giulia
Keep, Sarah
Adeyemi, Oluwapelumi
Bickerton, Erica
Kirk, James
AuthorAffiliation Cairo University Faculty of Veterinary Medicine, EGYPT
2 The Pirbright Institute, Woking, United Kingdom
3 The Francis Crick Institute, London, United Kingdom
1 New England Biolabs, Ipswich, Massachusetts, United States of America
AuthorAffiliation_xml – name: 2 The Pirbright Institute, Woking, United Kingdom
– name: Cairo University Faculty of Veterinary Medicine, EGYPT
– name: 3 The Francis Crick Institute, London, United Kingdom
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/39052682$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_1093_nar_gkae809
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Copyright Copyright: © 2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2024 Bilotti et al 2024 Bilotti et al
2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: Copyright: © 2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
– notice: COPYRIGHT 2024 Public Library of Science
– notice: 2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2024 Bilotti et al 2024 Bilotti et al
– notice: 2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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License Copyright: © 2024 Bilotti et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Competing Interests: I have read the journal’s policy and the authors of the manuscript have the following competing interests: When performing this research and drafting this manuscript, KB, APS, JMP, SKT, and GJSL were employees of New England Biolabs, a manufacturer and vendor of molecular biology reagents including DNA ligases and Type IIS restriction enzymes. New England Biolabs funded the work and paid the salaries of these authors. This does not alter our adherence to PLOS ONE policies on sharing data and materials. A patent has previously been filed by The Pirbright Institute to protect the intellectual property of the work surrounding the mutations in nsp 10 and nsp 14 (Patent name: Coronavirus, Number EP3172319B1, Authors: Erica Bickerton, Sarah Keep, and Paul Britton). This does not alter our adherence to PLOS ONE policies on sharing data and materials.
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SubjectTerms Animals
Artificial chromosomes
Assembly
Avian infectious bronchitis
Bacterial infections
Biology
Biology and Life Sciences
Breakpoints
Bronchitis
Coronavirus Infections - veterinary
Coronavirus Infections - virology
DNA
DNA damage
E coli
Escherichia coli
Escherichia coli - genetics
Food security
Food supply
Fragments
Genetics
Genome, Viral
Genomes
Genomic instability
Genomics
Immunization
Infections
Infectious bronchitis virus - genetics
Laboratories
Medicine and Health Sciences
Molecular biology
Mortality
Pathogens
Plasmids
Plasmids - genetics
Population genetics
Poultry
Poultry Diseases - virology
Research and Analysis Methods
Respiratory diseases
Reverse Genetics - methods
Severe acute respiratory syndrome coronavirus 2
Site fidelity
Vaccine development
Vaccines
Viruses
Zoonoses
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Title One-pot Golden Gate Assembly of an avian infectious bronchitis virus reverse genetics system
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http://dx.doi.org/10.1371/journal.pone.0307655
Volume 19
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