The expanded Inhibitor of Apoptosis gene family in oysters possesses novel domain architectures and may play diverse roles in apoptosis following immune challenge

Authors: WITKOP, ERIN - University Of Rhode Island; Proestou, Dina; GOMEZ-CHIARRI, MARTA - University Of Rhode Island

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/6/2021
Publication Date: 3/12/2022
Citation: Witkop, E.M., Proestou, D.A., Gomez-Chiarri, M. 2022. The expanded Inhibitor of Apoptosis gene family in oysters possesses novel domain architectures and may play diverse roles in apoptosis following immune challenge. BMC Genomics. https://doi.org/10.1186/s12864-021-08233-6.
DOI: https://doi.org/10.1186/s12864-021-08233-6

Interpretive Summary: Apoptosis plays important roles in immune and stress responses in all taxa. To better understand mechanisms of disease resistance and identify targets for genetic improvement in oysters, it is important to investigate apoptotic processes in response to disease challenge. More specifically, the inhibitor of apoptosis (IAP) gene family is a key regulator of apoptotic processes. This gene family is highly expanded in bivalve molluscs compared to other species, underscoring its importance in defending against disease, environmental stress, and self-harm. In this study, we quantified the expansion of the IAP gene family in the Eastern and Pacific oyster species, characterized the diversification of genes within the gene family at both the sequence domain and protein domain architecture levels, and explored the variation in gene expression patterns of the two species in response to independent immune challenges with a diversity of pathogens. Our analyses demonstrate that the regulation of apoptosis in response to immune challenge by the IAP gene family is complex and highly dependent on the host species, the resistance phenotype within the host species, and the specific pathogen involved in the host-pathogen interaction. Taken together, our results suggest that the evolution of an expanded and diverse set of genes involved in regulating apoptosis facilitates highly specialized oyster transcriptomic responses to pathogens in complex environments.

Technical Abstract: The Inhibitor of Apoptosis (IAP) gene family is expanded in Eastern and Pacific oysters. The evolution and functional importance of IAP expansion remains unknown. Phylogenetic analysis of molluscan IAP genes identified lineage specific gene expansion in bivalve species. IAP gene family expansion resulted from tandem duplication and was greater in Eastern (69) compared to Pacific (40) oysters. Functional domain analysis of IAP proteins identified 3 novel Baculoviral IAP Repeat domain types and 14 domain architecture types, 4 of which are not present in model organisms. Most IAP genes (76% of Eastern and 82% of Pacific) were expressed in response to immune challenge with varied pathogens. The two oyster species exhibited different patterns of IAP and apoptosis-related gene expression. The Eastern oyster expressed a unique set of IAP genes in response to each challenge while Pacific oyster IAP expression overlapped across all challenges. Apoptosis gene expression patterns clustered mainly by resistance/susceptibility of the oyster host to pathogens. Furthermore, co-expression of specific combinations of oyster IAP genes/transcripts/domain architecture types with apoptosis-related pathways is pathogen-dependent. The unprecedented sequence, domain, and protein domain architecture diversity observed in oyster IAPs, as well as the complex patterns of gene expression in response to varied immune challenges, suggests the expansion of this gene family facilitates complex regulation of immune responses in oysters.