Background <p>Insect-specific and insect-borne viruses (particularly RNA viruses) may pose a serious threat to global rice production. However, the effects of geographic genetic divergence and ecological viral communities in shaping insect viromes remain poorly understood. The striped stem borer, <i>Chilo suppressalis</i>—a notorious chewing pest widely distributed across China—serves as an ideal model to study RNA virus evolution and cross-species transmission dynamics in rice ecosystems.</p> Results <p>Meta-transcriptomic sequencing analysis of 48 <i>C. suppressalis</i> samples collected nationwide revealed four major geographic populations and identified 20 high-abundance viruses (15 novel). These include the widespread core virus Hangzhou sesamia inferens peribunyavirus 1 and Chilo suppressalis sedoreo-like virus 1, as well as several climate-adapted viruses that may represent extreme-environment specialists. Diversity analyses revealed that the geographic genetic divergence of <i>C. suppressalis</i> influences viral species composition but not the overall virome structure. Parallel sequencing of 5 <i>Cotesia chilonis</i> (endoparasitoid) samples revealed 8 high-abundance viruses (5 novel). Significant variations in distribution patterns, viral loads, and vsiRNA profiles within <i>C. suppressalis–C. chilonis</i> parasitic system suggested host-driven adaptive evolution of these viruses. Co-occurrence network analysis demonstrated that sympatric species (such as <i>Sesamia inferens</i> and rice planthoppers) and their host plant, rice, significantly influence <i>C. suppressalis</i> virome composition, highlighting cross-kingdom viral transmission dynamics.</p> Conclusions <p>This study elucidates the synergistic roles of geographical divergence and ecological viral communities in driving virome diversity in <i>C. suppressalis</i>. Our findings advance the understanding of virus<b>-</b>host coevolution in agricultural ecosystems and provide a framework for developing integrated strategies targeting both insect pests and their viral pathogens in rice cultivation.</p> <p><MediaObject ID="MOESM4"> <VideoObject FileRef="MediaObjects/40168_2026_2407_MOESM4_ESM.mp4" VideoID="EQe2ZtzNGg2MXTmzj3K2mu"> <Caption Language="En" xml:lang="en"> <CaptionContent> <p>Video Abstract</p> </CaptionContent> </Caption> </VideoObject> </MediaObject></p>

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Geographic genetic divergence and ecological viral communities shape the virome of Chilo suppressalis

  • Jia-Bao Lu,
  • Ying Tian,
  • Yi-Yuan Li,
  • Yu-Hua Qi,
  • Fang He,
  • Peng-Peng Ren,
  • Hai-Jian Huang,
  • Ji-Chong Zhuo,
  • Qing-Ling Hu,
  • Gang Lu,
  • Qian-Zhuo Mao,
  • Jian-Ping Chen,
  • Jun-Min Li,
  • Chuan-Xi Zhang

摘要

Background

Insect-specific and insect-borne viruses (particularly RNA viruses) may pose a serious threat to global rice production. However, the effects of geographic genetic divergence and ecological viral communities in shaping insect viromes remain poorly understood. The striped stem borer, Chilo suppressalis—a notorious chewing pest widely distributed across China—serves as an ideal model to study RNA virus evolution and cross-species transmission dynamics in rice ecosystems.

Results

Meta-transcriptomic sequencing analysis of 48 C. suppressalis samples collected nationwide revealed four major geographic populations and identified 20 high-abundance viruses (15 novel). These include the widespread core virus Hangzhou sesamia inferens peribunyavirus 1 and Chilo suppressalis sedoreo-like virus 1, as well as several climate-adapted viruses that may represent extreme-environment specialists. Diversity analyses revealed that the geographic genetic divergence of C. suppressalis influences viral species composition but not the overall virome structure. Parallel sequencing of 5 Cotesia chilonis (endoparasitoid) samples revealed 8 high-abundance viruses (5 novel). Significant variations in distribution patterns, viral loads, and vsiRNA profiles within C. suppressalis–C. chilonis parasitic system suggested host-driven adaptive evolution of these viruses. Co-occurrence network analysis demonstrated that sympatric species (such as Sesamia inferens and rice planthoppers) and their host plant, rice, significantly influence C. suppressalis virome composition, highlighting cross-kingdom viral transmission dynamics.

Conclusions

This study elucidates the synergistic roles of geographical divergence and ecological viral communities in driving virome diversity in C. suppressalis. Our findings advance the understanding of virus-host coevolution in agricultural ecosystems and provide a framework for developing integrated strategies targeting both insect pests and their viral pathogens in rice cultivation.

Video Abstract