Comprehensive characterization of non-retroviral endogenous viral elements in the rice pest Chilo suppressalis

Non-retroviral endogenous viral elements (nrEVEs) are "molecular fossils" in eukaryotes that offer key molecular evidence into virus-host coevolution, particularly in insects. The striped rice stem borer (Chilo suppressalis), one of the most notorious chewing rice pests, is widely distributed across China. By integrating meta-transcriptome, small RNA (sRNA) sequencing, and the published C. suppressalis genomic data, a comprehensive characterization of nrEVEs in this species was revealed.

Fifteen nrEVEs were identified in the C. suppressalis genome, comprising 13 Orthomyxoviridae-derived and two Rhabdoviridae-derived viral sequences (designated CsOrEVE1-13 and CsRhEVE1-2). These elements are integrated in either forward or reverse orientation across multiple chromosomes, and share 49-77% sequence identity with known exogenous viruses. Phylogenetic analyses revealed that most CsOrEVEs cluster closely with the Quaranjavirus clade, suggesting historical infections by viruses of this genus. Transcriptomic profiling revealed distinct expression patterns: CsOrEVE3 and CsOrEVE5 showed developmental stage-specificity; CsOrEVE3, CsOrEVE6, and CsOrEVE11 exhibited tissue-specificity; and CsOrEVE1, CsOrEVE3, and CsOrEVE6 were expressed in a geographic population-specific manner. Twelve nrEVEs in C. suppressalis were located within transcripts predicted to contain intact open reading frames. Among these, CsOrEVE11, CsOrEVE12, and CsOrEVE13 were found within intron-containing host transcripts, suggesting their potential as candidates for molecular domestication. sRNA sequencing detected abundant piRNA-like reads derived from most nrEVEs. Furthermore, various integration-related domains such as retrotransposons in the flanking regions of these nrEVEs may serve as critical evidence to help hypothesize their origins.

This study presents a comprehensive characterization of nrEVEs in C. suppressalis through bioinformatic characterization, demonstrating their association with host mRNAs and their potential important roles. Our findings advance the understanding of long-term virus-host coevolution and genomic structure formation in C. suppressalis, and establish a theoretical foundation for further research on the functions of nrEVEs.