Differential gene expression in a tripartite interaction: Drosophila , Spiroplasma and parasitic wasps

• Published in: PeerJ (San Francisco, CA) CA), 2021-03, Vol.9, p.e11020-e11020, Article e11020
• Main Authors: Higareda Alvear, Victor Manuel, Mateos, Mariana, Cortez, Diego, Tamborindeguy, Cecilia, Martinez-Romero, Esperanza
• Format: Article
• Language: English
• Subjects: Bacteria; Bioinformatics; Competition; Drosophila; Ecology; Entomology; Females; Gene expression; Genomes; Immune response; Immunity; Insects; Males; Metatranscriptome; Molecular Biology; Natural enemies; Parasites; Parasitic wasp; Parasitism; Pest resistance; Protection; Recipes; Ribonucleic acid; RNA; rRNA; Spiroplasma; Symbionts; Transcription; Zoology
• ISSN: 2167-8359; 2167-8359
• DOI: 10.7717/peerj.11020

Several facultative bacterial symbionts of insects protect their hosts against natural enemies. strain Mel (hereafter ), a male-killing heritable symbiont of , confers protection against some species of parasitic wasps. Several lines of evidence suggest that -encoded ribosome inactivating proteins (RIPs) are involved in the protection mechanism, but the potential contribution of the fly-encoded functions (e.g., immune response), has not been deeply explored. Here we used RNA-seq to evaluate the response of to infection by and parasitism by the -susceptible wasp , and the -resistant wasp sp. In addition, we used quantitative (q)PCR to evaluate the transcript levels of the -encoded Ribosomal inactivation protein (RIP) genes. In the absence of infection, we found evidence of immune activation by sp., but not by , which in turn negatively influenced functions associated with male gonad development. As expected for a symbiont that kills males, we detected extensive downregulation in the -infected treatments of genes known to have male-biased expression. We detected very few genes whose expression patterns appeared to be influenced by the interaction, and these genes are not known to be associated with immune response. For most of these genes, parasitism by (in the absence of ) caused an expression change that was at least partly reversed when both and were present. It is unclear whether such genes are involved in the -mediated mechanism that leads to wasp death and/or fly rescue. Nonetheless, the expression pattern of some of these genes, which reportedly undergo expression shifts during the larva-to-pupa transition, is suggestive of an influence of on the development time of -parasitized flies. One of the five RIP genes (RIP2) was consistently highly expressed independently of wasp parasitism, in two substrains of Mel. Finally, the RNAseq data revealed evidence consistent with RIP-induced damage in the ribosomal (r)RNA of the -susceptible, but not the -resistant, wasp. Acknowledging the caveat that we lacked adequate power to detect the majority of DE genes with fold-changes lower than 3, we conclude that immune priming is unlikely to contribute to the -mediated protection against wasps, and that the mechanism by which . resists/tolerates does not involve inhibition of RIP transcription.