IAP (Inhibitor-of-Apoptosis Protein) gene family expansion and functional diversification in aphids

Apoptosis is a widespread form of regulated cell death, controlled by a genetically-encoded machinery conserved in almost all metazoan clades. In the highly diverse group of insects, apoptotic pathways have been characterized in only a few dipteran and lepidopteran species, where they have been shown to be essential for development, metamorphosis and immunity-related processes. The lack of studies in other insect orders clearly limits our understanding of the role of apoptosis in insects’ lives. In this study, we combined phylogenetic analyses and conserved domain identification to annotate the apoptosis pathway in a hemipteran model: the pea aphid Acyrthosiphon pisum. We found that the executive part of the pathway is incomplete, with homologs for only 4 out of the 8 proteins present in Drosophila melanogaster, while the inhibitory part underwent a large expansion, with over 30 Inhibitor-of-Apoptosis Proteins (IAPs) in contrast to the 4 to 7 found in other insect species. Tissue-specific qRT-PCR and RNAseq analyses have shown that, in senescent aphids, only two apoptotic effectors are induced in bacteriocytes, the specialized cells housing symbiotic bacteria, while several apoptosis inhibitors are concomitantly over-expressed. This provides a possible mechanism whereby apoptosis is prevented in these cells, enabling the emergence of a novel cell death process. We have confirmed the anti-apoptotic role of these bacteriocyte cell death-associated IAPs in heterologous expression experiments using a tractable in vivo model, the drosophila developing eye. These results suggest that a restricted set of aphid IAPs have a key role in bacteriocyte homeostasis. Other aphid IAPs are differentially expressed in different life stages and tissues, suggesting an as yet not understood functional diversification. Interestingly, this IAP functional diversification is expected to also occur in other aphid species as, using comparative phylogenomics analyses, we have demonstrated that IAP expansion is widespread in aphid lineages.