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.

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.

Metrics

  • 1,542
    views
  • 289
    downloads
  • 8
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Ecology
    2. Neuroscience
    Kathleen T Quach, Gillian A Hughes, Sreekanth H Chalasani
    Research Article

    Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.