Diversity and evolution analysis of RNA viruses in three wheat aphid species

Abstract

Background: Although advances in metagenomics, viral diversity and non-retroviral endogenous viral elements (EVEs) in wheat aphids remain underexplored. By analyzing 470 publicly available datasets and one laboratory-generated transcriptome, the RNA virome and EVEs in the genomes of Sitobion avenae, Schizaphis graminum, and Rhopalosiphum padi were systematically investigated.

Results: We identified 43 RNA viruses, including 12 novel and 31 known RNA viruses. These viruses were widely distributed and abundant in different geographic populations of three wheat aphid species. +ssRNA viruses were the dominant type of aphid viruses. Besides, 90 EVEs were discovered in the genomes of three aphid species. In addition, the EVEs exhibit potential domestication and novel functional roles within aphid genomes.

Conclusions: This study expands the understanding of RNA virus diversity in aphids and provides valuable insights into the potential functions of EVEs in virus-host coevolution.

Keywords: Endogenous viral elements; Insect-specific viruses; RNA virome; Wheat aphids.

Fig. 1

Genomic structures of novel RNA viruses identified in the three wheat aphid species. The viruses were classified into two groups: +ssRNA viruses (A) and -ssRNA viruses (B). Each virus was listed according to its taxonomic family. Conserved functional domains are color-coded, with the domain names indicated at the bottom of the figure. RdRP, RNA-dependent RNA polymerase; CP, coat protein; G, glycoprotein; NP, nucleoprotein. GenBank accession numbers are listed in Table 1

Fig. 2

Phylogenetic analysis of the identified wheat aphid RNA viruses. The phylogenetic tree for Iflaviridae [A(I)], Solinviviridae [A(II)], Negevirus (B), Tombusviridae (C), Fusariviridae (D), Narnaviridae (E), Lispiviridae (F), Rhabdoviridae (G) and Phenuiviridae (H) are based on the maximum likelihood method and inferred from conserved viral RdRP domains. Novel RNA viruses are shown in red font. Nodes with bootstrap values > 50% are marked with blue circles. In panels A, taxonomic overview of the order Picornavirales is shown in the center, and close-up views of two clusters shown in the dashed boxes with arrows. The detailed virus names in each branch of the phylogenetic tree are shown in Fig. S1 and the GenBank accession numbers of these viruses are listed in Table S4

Fig. 3

Analysis of RNA virome abundance in different datasets of three aphid species. Distribution of RNA viruses in Sitobion avenae (A), Schizaphis graminum (B), and Rhopalosiphum padi (C) across different databases. Blue indicates the absence of viral abundance, while other colors represent presence of viral abundance. The abundance ranges indicated by transcripts per million (TPM)

Fig. 4

Identification of endogenous viral elements (EVEs) in the genomes of three wheat aphid species. (A–C) Alignment of EVEs from the genomes of Sitobion avenae (A), Schizaphis graminum (B), and Rhopalosiphum padi (C) with distinct viral genomes. The EVE names are shown below each type of viral genomes and the detailed information of these EVEs is listed in Table S5. RdRP, RNA-dependent RNA polymerase; L, large protein; CP, coat protein; G, glycoprotein; N, nucleoprotein. (D and E) Phylogenetic analysis of EVEs and related exogenous viruses. The maximum likelihood algorithm was used to construct phylogenetic trees for viral RdRP sequences in Partitiviridae (D) and G sequences in Chuviridae (E) and the corresponding EVE aa sequences. EVEs are shown in red font. Nodes with bootstrap values > 50% are marked with blue circles. Scale bars represent the percentage divergence. The viral sequences used for phylogenetic tree construction are listed in Table S4

Fig. 5

Transcription expression analyses of EVEs in different geographic populations of three wheat aphid species. (A) Heatmap displays the abundance of transcript reads derived from EVEs of Sitobion avenae, Schizaphis graminum, and Rhopalosiphum padi across wheat aphid datasets from various origins. Abbreviations for the datasets submitters and other related details are listed in Table S1. (B–D) Schematic diagrams represent the position and coverage of transcripts containing EVEs within the genome of S. avenae (B), S. graminum (C), and R. padi (D). The size distribution of small RNAs derived from each of the EVEs is displayed on the left panel. Predicted open reading frames (ORFs) are indicated with red double-headed arrows