Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
Research Article

Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus

Juan Pu, Shuoguo Wang, Yanbo Yin, Guozhong Zhang, Robert A. Carter, Jinliang Wang, Guanlong Xu, Honglei Sun, Min Wang, Chu Wen, Yandi Wei, Dongdong Wang, Baoli Zhu, Gordon Lemmon, Yuannian Jiao, Susu Duan, Qian Wang, Qian Du, Meng Sun, Jinnan Bao, Yipeng Sun, Jixun Zhao, Hui Zhang, Gang Wu, Jinhua Liu, and Robert G. Webster
PNAS first published December 29, 2014; https://doi.org/10.1073/pnas.1422456112
Juan Pu
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
bDepartment of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Shuoguo Wang
cDepartment of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yanbo Yin
dCollege of Animal Science and Veterinary Medicine, Qingdao Agricultural University, Qingdao 266109, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Guozhong Zhang
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert A. Carter
cDepartment of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jinliang Wang
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Guanlong Xu
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Honglei Sun
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Min Wang
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Chu Wen
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yandi Wei
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Dongdong Wang
dCollege of Animal Science and Veterinary Medicine, Qingdao Agricultural University, Qingdao 266109, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Baoli Zhu
eChinese Academy of Sciences Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gordon Lemmon
cDepartment of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yuannian Jiao
cDepartment of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Susu Duan
bDepartment of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Qian Wang
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Qian Du
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Meng Sun
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jinnan Bao
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yipeng Sun
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jixun Zhao
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hui Zhang
fDepartment of Biostatistics, St. Jude Children's Research Hospital, Memphis, TN 38105
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gang Wu
cDepartment of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jinhua Liu
aKey Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: ljh@cau.edu.cn robert.webster@stjude.org
Robert G. Webster
bDepartment of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN 38105;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: ljh@cau.edu.cn robert.webster@stjude.org
  1. Contributed by Robert G. Webster, November 26, 2014 (sent for review October 22, 2014)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Significance

The emergence of human infection with a novel H7N9 avian influenza reassortant in China raises a pandemic concern. However, it is not fully understood how these H9N2 chicken viruses facilitated the genesis of the novel H7N9 viruses. Here we show that a “fittest” genotype (G57) emerged with changed antigenicity and improved adaptability in chickens. It became predominant in vaccinated farm chickens and caused widespread outbreaks before the H7N9 virus emergence, increasing reassortment between H9N2 and other subtype viruses and finally providing all of their internal genes to the novel H7N9 viruses. The prevalence and variation of H9N2 influenza virus in farmed poultry could provide an important early warning of the emergence of novel reassortants with pandemic potential.

Abstract

The emergence of human infection with a novel H7N9 influenza virus in China raises a pandemic concern. Chicken H9N2 viruses provided all six of the novel reassortant’s internal genes. However, it is not fully understood how the prevalence and evolution of these H9N2 chicken viruses facilitated the genesis of the novel H7N9 viruses. Here we show that over more than 10 y of cocirculation of multiple H9N2 genotypes, a genotype (G57) emerged that had changed antigenicity and improved adaptability in chickens. It became predominant in vaccinated farm chickens in China, caused widespread outbreaks in 2010–2013 before the H7N9 viruses emerged in humans, and finally provided all of their internal genes to the novel H7N9 viruses. The prevalence and variation of H9N2 influenza virus in farmed poultry could provide an important early warning of the emergence of novel reassortants with pandemic potential.

  • H9N2
  • H7N9
  • chicken influenza virus
  • genotype
  • infectivity

Footnotes

  • ↵1J.P., S.W., and Y.Y. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: ljh{at}cau.edu.cn or robert.webster{at}stjude.org.
  • Author contributions: J.P., G.Z., J.Z., and J.L. designed research; J.P., Y.Y., G.Z., J.W., G.X., H.S., M.W., C.W., Y.W., D.W., B.Z., Y.J., Q.W., Q.D., M.S., and J.B. performed research; J.P., S.W., G.Z., R.A.C., J.W., M.W., G.L., Y.S., J.Z., H.Z., G.W., J.L., and R.G.W. analyzed data; and J.P., S.D., G.W., J.L., and R.G.W. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences generated in this study have been deposited in the Genbank database (accession nos. are listed in Table S3).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1422456112/-/DCSupplemental.

Next
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
H9N2 evolution in the genesis of H7N9 virus
Juan Pu, Shuoguo Wang, Yanbo Yin, Guozhong Zhang, Robert A. Carter, Jinliang Wang, Guanlong Xu, Honglei Sun, Min Wang, Chu Wen, Yandi Wei, Dongdong Wang, Baoli Zhu, Gordon Lemmon, Yuannian Jiao, Susu Duan, Qian Wang, Qian Du, Meng Sun, Jinnan Bao, Yipeng Sun, Jixun Zhao, Hui Zhang, Gang Wu, Jinhua Liu, Robert G. Webster
Proceedings of the National Academy of Sciences Dec 2014, 201422456; DOI: 10.1073/pnas.1422456112

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
H9N2 evolution in the genesis of H7N9 virus
Juan Pu, Shuoguo Wang, Yanbo Yin, Guozhong Zhang, Robert A. Carter, Jinliang Wang, Guanlong Xu, Honglei Sun, Min Wang, Chu Wen, Yandi Wei, Dongdong Wang, Baoli Zhu, Gordon Lemmon, Yuannian Jiao, Susu Duan, Qian Wang, Qian Du, Meng Sun, Jinnan Bao, Yipeng Sun, Jixun Zhao, Hui Zhang, Gang Wu, Jinhua Liu, Robert G. Webster
Proceedings of the National Academy of Sciences Dec 2014, 201422456; DOI: 10.1073/pnas.1422456112
Digg logo Reddit logo Twitter logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 118 (3)
Current Issue

Submit

Sign up for Article Alerts

Jump to section

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Abstract depiction of a guitar and musical note
Science & Culture: At the nexus of music and medicine, some see disease treatments
Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s.
Image credit: Shutterstock/agsandrew.
Scientist looking at an electronic tablet
Opinion: Standardizing gene product nomenclature—a call to action
Biomedical communities and journals need to standardize nomenclature of gene products to enhance accuracy in scientific and public communication.
Image credit: Shutterstock/greenbutterfly.
One red and one yellow modeled protein structures
Journal Club: Study reveals evolutionary origins of fold-switching protein
Shapeshifting designs could have wide-ranging pharmaceutical and biomedical applications in coming years.
Image credit: Acacia Dishman/Medical College of Wisconsin.
White and blue bird
Hazards of ozone pollution to birds
Amanda Rodewald, Ivan Rudik, and Catherine Kling talk about the hazards of ozone pollution to birds.
Listen
Past PodcastsSubscribe
Goats standing in a pin
Transplantation of sperm-producing stem cells
CRISPR-Cas9 gene editing can improve the effectiveness of spermatogonial stem cell transplantation in mice and livestock, a study finds.
Image credit: Jon M. Oatley.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Latest Articles
  • Archive

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490