Abstract
Aldehyde oxidases (AOXs) are common detoxifying enzymes in several organisms. In insects, AOXs act in xenobiotic metabolism and as odorant-degrading enzymes (ODEs). These last appear as crucial enzymes in the life cycle of insects, helping to reset their olfactory system, particularly in lepidopterans, which fulfill important ecological roles (e.g., pollination or destructive life cycles). A comprehensive understanding of their olfactory system has provided opportunities to study key chemosensory proteins. However, no significant advance has been made around lepidopteran AOXs research, and even less around butterflies, a recently evolved lineage. In this study we have identified novel AOX gene families in moths and butterflies in order to understand their role as ODEs. Eighteen genomes from both moths and butterflies were used for phylogenetics, molecular evolution and sequence analyses. We identified 164 AOXs, from which 91 are new. Their phylogeny showed two main clades that are potentially related to odorant-degrading function, where both moths and butterflies have AOXs. A first ODE-related clade seems to have a non-ditrysian origin, likely related to plant volatiles. A second ODE-related clade could be more pheromone-biased. Molecular evolution analysis suggests a slight purifying selection process, though a number of sites appeared under positive selection. ODE-related AOXs have changed a phenylalanine residue by proline in the active site. Finally, this study could serve as a reference for further evolutionary and functional studies around Lepidopteran AOXs.
Highlights
The study of gene evolution in insects has provided outstanding advances in the understanding of evolutionary processes, such as expansion or contraction of gene families (Li et al, 2019)
It is worth noting that the amount and length of aldehyde oxidases (AOXs) genes might be dependent on genome sequencing and annotation quality, previous estimates should be taken into account with caution
Reports about insect AOXs and their function toward aldehydes took more than 20 years to be published again, when A. transitella AOX2 (AtraAOX2) was comprehensively studied (Choo et al, 2013)
Summary
The study of gene evolution in insects has provided outstanding advances in the understanding of evolutionary processes, such as expansion or contraction of gene families (Li et al, 2019). Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) function as transporters that carry odorants across the sensillar lymph (Zhou, 2010; Leal, 2013) These odorants reach an heteromeric complex of receptors, such as odorant receptors (ORs), an odorant receptor co-receptor (Orco) and a sensory neuron membrane protein (SNMP), as recently reported (Zhang et al, 2020), to unleash depolarization in olfactory neuron membranes that triggers a behavioral response (Kaissling, 2013). Along with these olfactory proteins, odorant-degrading enzymes (ODEs), such as carboxylesterases (CXEs), glutathione-S-transferases (GSTs) and aldehyde oxidases (AOXs), are responsible for resetting the insect olfactory system through the degradation of odorant molecules (Chertemps and Meïbèche, 2021; Godoy et al, 2021)
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