Abstract
The insect chemosensory repertoires of Odorant Receptors (ORs) and Gustatory Receptors (GRs) together represent one of the largest families of ligand-gated ion channels. Previous analyses have identified homologous 'Gustatory Receptor-Like' (GRL) proteins across Animalia, but the evolutionary origin of this novel class of ion channels is unknown. We describe a survey of unicellular eukaryotic genomes for GRLs, identifying several candidates in fungi, protists and algae that contain many structural features characteristic of animal GRLs. The existence of these proteins in unicellular eukaryotes, together with ab initio protein structure predictions, provide evidence for homology between GRLs and a family of uncharacterized plant proteins containing the DUF3537 domain. Together, our analyses suggest an origin of this protein superfamily in the last common eukaryotic ancestor.
Highlights
The insect chemosensory receptor superfamily, comprising Odorant Receptors (ORs) and GustatoryReceptors (GRs), forms a critical molecular interface between diverse chemical signals in the environment and neural activity patterns that evoke behavioral responses (Benton, 2015; Joseph and Carlson, 2015; Robertson, 2019; Rytz et al, 2013; van Giesen and Garrity, 2017)
We used diverse insect ORs and GRs, other animal Gustatory Receptor-Like’ (GRL) and plant Domain of Unknown Function 3537 (DUF3537) families as sequence queries in BLAST searches of protein and genomic sequence databases of unicellular organisms
Significant hits were subjected to further assessment to exclude spurious similarities, retaining those that fulfilled most or all of the following criteria: (i) reciprocal BLAST using a candidate sequence as query identified a known GRL or DUF3537 member as a top hit; (ii) ~ 350–500 amino acids long, similar to GRLs/DUF3537 proteins; (iii) predicted seven TM domains; (iv) intracellular N-terminus; (v) longer intracellular loops than extracellular loops
Summary
The insect chemosensory receptor superfamily, comprising Odorant Receptors (ORs) and GustatoryReceptors (GRs), forms a critical molecular interface between diverse chemical signals in the environment and neural activity patterns that evoke behavioral responses (Benton, 2015; Joseph and Carlson, 2015; Robertson, 2019; Rytz et al, 2013; van Giesen and Garrity, 2017). In contrast to vertebrate olfactory and taste receptors, which belong to the G protein-coupled receptor (GPCR) superfamily of seven TM domain proteins (Glezer and Malnic, 2019; Yarmolinsky et al, 2009), insect ORs and GRs have the opposite topology, with an intracellular N-terminus (Benton et al, 2006; Lundin et al, 2007) Functional analyses of these proteins in heterologous expression systems indicate that they form ligandgated ion channels (Butterwick et al, 2018; Sato et al, 2008; Sato et al, 2011; Wicher et al., 2008).
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