Rapid spread of a densovirus in a major crop pest following wide-scale adoption of Bt-cotton in China

  1. Yutao Xiao
  2. Wenjing Li
  3. Xianming Yang
  4. Pengjun Xu
  5. Minghui Jin
  6. He Yuan
  7. Weigang Zheng
  8. Mario Soberón
  9. Alejandra Bravo
  10. Kenneth Wilson
  11. Kongming Wu  Is a corresponding author
  1. Chinese Academy of Agricultural Sciences, China
  2. Hubei Academy of Agricultural Sciences, China
  3. Universidad Nacional Autónoma de México, Mexico
  4. Lancaster University, United Kingdom

Abstract

Bacillus thuringiensis (Bt) crops have been widely planted and the effects of Bt-crops on populations of the target and non-target insect pests have been well studied. However, the effects of Bt-crops exposure on microorganisms that interact with crop pests have not previously been quantified. Here, we use laboratory and field data to show that infection of Helicoverpa armigera with a densovirus (HaDV2) is associated with its enhanced growth and tolerance to Bt-cotton. Moreover, field monitoring showed a much higher incidence of cotton bollworm infection with HaDV2 in regions cultivated with Bt-cotton than in regions without it, with the rate of densovirus infection increasing with increasing use of Bt-cotton. RNA-seq suggested tolerance to both baculovirus and Cry1Ac were enhanced via the immune-related pathways. These findings suggest that exposure to Bt-crops has selected for beneficial interactions between the target pest and a mutualistic microorganism that enhances its performance on Bt-crops under field conditions.

Data availability

RNA-seq data have been deposited in NCBI, see supplementary table 8.All data generated or analysed during this study are included in the manuscript and supplementary file.

The following data sets were generated

Article and author information

Author details

  1. Yutao Xiao

    Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
    Competing interests
    No competing interests declared.
  2. Wenjing Li

    Institute of Plant Protection and Soil Fertility, Hubei Academy of Agricultural Sciences, Wuhan, China
    Competing interests
    No competing interests declared.
  3. Xianming Yang

    Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    No competing interests declared.
  4. Pengjun Xu

    Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China
    Competing interests
    No competing interests declared.
  5. Minghui Jin

    Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
    Competing interests
    No competing interests declared.
  6. He Yuan

    Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
    Competing interests
    No competing interests declared.
  7. Weigang Zheng

    Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
    Competing interests
    No competing interests declared.
  8. Mario Soberón

    Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo, Mexico
    Competing interests
    Mario Soberón, coauthor of a patent on modified Bt toxins, Suppression of Resistance in Insects to Bacillus thuringiensis Cry Toxins.
  9. Alejandra Bravo

    Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo, Mexico
    Competing interests
    Alejandra Bravo, coauthor of a patent on modified Bt toxins, Suppression of Resistance in Insects to Bacillus thuringiensis Cry Toxins.
  10. Kenneth Wilson

    Lancaster Environment Centre, Lancaster University, Lancaster, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5264-6522
  11. Kongming Wu

    Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
    For correspondence
    wukongming@caas.cn
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3555-4292

Funding

the Key Project for Breeding Genetic Modified Organisms (2019ZX08012004)

  • Kongming Wu

the Key Project for Breeding Genetic Modified Organisms (2016ZX08012004)

  • Kongming Wu

Biotechnology and Biological Sciences Research Council (BB/L026821/1)

  • Kenneth Wilson

UK Research Council Global Challenges Research Fund Grant (BB/P023444/1)

  • Kenneth Wilson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David Heckel, MPI Chemical Ecology, Germany

Version history

  1. Received: January 26, 2021
  2. Preprint posted: February 10, 2021 (view preprint)
  3. Accepted: July 13, 2021
  4. Accepted Manuscript published: July 15, 2021 (version 1)
  5. Version of Record published: July 30, 2021 (version 2)

Copyright

© 2021, Xiao et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Yutao Xiao
  2. Wenjing Li
  3. Xianming Yang
  4. Pengjun Xu
  5. Minghui Jin
  6. He Yuan
  7. Weigang Zheng
  8. Mario Soberón
  9. Alejandra Bravo
  10. Kenneth Wilson
  11. Kongming Wu
(2021)
Rapid spread of a densovirus in a major crop pest following wide-scale adoption of Bt-cotton in China
eLife 10:e66913.
https://doi.org/10.7554/eLife.66913

Share this article

https://doi.org/10.7554/eLife.66913

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