Unravelling the Complex Duplication History of Deuterostome Glycerol Transporters

Abstract

<jats:p>Transmembrane glycerol transport is an ancient biophysical property that evolved in selected subfamilies of water channel (aquaporin) proteins. Here, we conducted broad level genome (&gt;550) and transcriptome (&gt;300) analyses to unravel the duplication history of the glycerol-transporting channels (glps) in Deuterostomia. We found that tandem duplication (TD) was the major mechanism of gene expansion in echinoderms and hemichordates, which, together with whole genome duplications (WGD) in the chordate lineage, continued to shape the genomic repertoires in craniates. Molecular phylogenies indicated that aqp3-like and aqp13-like channels were the probable stem subfamilies in craniates, with WGD generating aqp9 and aqp10 in gnathostomes but aqp7 arising through TD in Osteichthyes. We uncovered separate examples of gene translocations, gene conversion, and concerted evolution in humans, teleosts, and starfishes, with DNA transposons the likely drivers of gene rearrangements in paleotetraploid salmonids. Currently, gene copy numbers and BLAST are poor predictors of orthologous relationships due to asymmetric glp gene evolution in the different lineages. Such asymmetries can impact estimations of divergence times by millions of years. Experimental investigations of the salmonid channels demonstrated that approximately half of the 20 ancestral paralogs are functional, with neofunctionalization occurring at the transcriptional level rather than the protein transport properties. The combined findings resolve the origins and diversification of glps over &gt;800 million years old and thus form the novel basis for proposing a pandeuterostome glp gene nomenclature.</jats:p>

Lineage-level Divergence of Copepod Glycerol Transporters and the Emergence of Isoform-specific Trafficking Regulation

“…A review of the glp gene complement in a more distantly related chelicerate, the Atlantic horshoe crab (Limulus polyphemus) also reveals eight paralogs encoded in the genome of this species. As previously reported for vertebrates 2,15,30 , the basis for some of the higher glp copy numbers in chelicerates such as L.…”

“…as described previously 47 to match each peptide fragment, and finally concatenated to construct a coding sequence (CDS) for each gene or transcript as described previously 15,45 . Prior to Bayesian (Mr Bayes v3.2.2; 48 analyses, data sets of the deduced amino acids were aligned using the L-INS-I or G-INS-I algorithms of MAFFT v7.453 49 , and converted to codon alignments using Pal2Nal 50 as described previously 15,45 . Bayesian phylogenetic analyses with model parameters nucmodel = 4by4, nst = 2, rates = gamma were performed on the codon alignments following removal of the N-and C-termini and gapped regions containing less than three sequences.…”

“…In contrast to the water-selective branches of aquaporins, which typically display narrow selectivity filters composed of four aromatic arignine (ar/R) residues [6][7][8][9] , the crosssectional sizes of the Glp selectivity filters are broader and thus facilitate the passage of larger molecules [10][11][12] . Evolutionary studies have shown that Glps are widespread in both prokrayotic and eukaryotic organisms, but are not ubiquitous, having been lost in certain lineages of protists, plants and insects 2,4,[13][14][15] . In the two latter lineages of plants and insects, Glps were supplanted by other members of the aquaporin superfamily, either via horizontal gene transfer of nodulin 26-like integral proteins (NIPs) and GlpF-like intrinsic proteins (GIPs) in plants 2,4,13,16,17 or through functional co-option and molecular supplantation by the entomoglyceroporins (Eglps) in hemipteran and holometabolous insects 14,18 .…”

Parallel duplication and loss of aquaporin-coding genes during the ‘out of the sea’ transition as potential key drivers of animal terrestrialization

“…Aquaporin-coding genes nomenclature between animal phyla is challenging due to the lack of consistency in the different studies (Benoit et al, 2014;Kosicka, Grobys, Kmita, Lesicki, & Pieńkowska, 2016;Kosicka, Lesicki, & Pieńkowska, 2020;Mucciolo et al, 2021;Stavang et al, 2015;Yilmaz et al, 2020). This conflict worsens when considering papers on the identification of aquaporins of isolated species without taking their evolutionary history into account (Grohme et al, 2013;Huang et al, 2007).…”

Bioinspired Freeze‐Tolerant Soft Materials: Design, Properties, and Applications

“…To tolerate osmotic stress variations that occur due to large vapor pressures, many living organisms are known to produce important osmoprotectants (e.g., urea, amino acid, sugar, polyhydric alcohol, and betaine) that can increase cell membrane permeability to water, modulate the rate of cell shrinkage, and thus stabilize the osmotic stress. [ 2,11–14 ] Furthermore, excreting noncolligative substrates such as ice‐binding proteins (IBPs) can significantly impede the ice growth process, which also plays an important role in the survival of some animals and plants during winter (Figure 1c). [ 8,15 ] For example, many species of fishes (e.g., icefish, winter flounder, herring, and ocean pout) have evolved to develop different types of antifreeze proteins (AFPs) in their body fluids.…”