Aquaporin Evolution in Fishes

Aquaporins represent a primordial group of transmembrane solvent channels that have been documented throughout the living biota. This facet alone emphasizes the positive selection pressure for proteins associated with intracellular fluid homeostasis. Amongst extant Eukaryota the highest gene copy number can be found in plants and teleosts, a feature that reflects the genomic duplication history in both groups. In this minireview we discuss the discovery, structure, duplication, and diversification of the aquaporin superfamily. We focus on teleosts as the main models, but include data available for other organisms to provide a broader perspective

Evolution and differential expression of a vertebrate vitellogenin gene cluster

<p>Abstract</p> <p>Background</p> <p>The multiplicity or loss of the vitellogenin (<it>vtg</it>) gene family in vertebrates has been argued to have broad implications for the mode of reproduction (placental or non-placental), cleavage pattern (meroblastic or holoblastic) and character of the egg (pelagic or benthic). Earlier proposals for the existence of three forms of vertebrate <it>vtgs </it>present conflicting models for their origin and subsequent duplication.</p> <p>Results</p> <p>By integrating phylogenetics of novel <it>vtg </it>transcripts from old and modern teleosts with syntenic analyses of all available genomic variants of non-metatherian vertebrates we identify the gene orthologies between the Sarcopterygii (tetrapod branch) and Actinopterygii (fish branch). We argue that the vertebrate <it>vtg </it>gene cluster originated in proto-chromosome m, but that <it>vtg </it>genes have subsequently duplicated and rearranged following whole genome duplications. Sequencing of a novel fourth <it>vtg </it>transcript in labrid species, and the presence of duplicated paralogs in certain model organisms supports the notion that lineage-specific gene duplications frequently occur in teleosts. The data show that the <it>vtg </it>gene cluster is more conserved between acanthomorph teleosts and tetrapods, than in ostariophysan teleosts such as the zebrafish. The differential expression of the labrid <it>vtg </it>genes are further consistent with the notion that neofunctionalized Aa-type <it>vtgs </it>are important determinants of the pelagic or benthic character of the eggs in acanthomorph teleosts.</p> <p>Conclusion</p> <p>The vertebrate <it>vtg </it>gene cluster existed prior to the separation of Sarcopterygii from Actinopterygii >450 million years ago, a period associated with the second round of whole genome duplication. The presence of higher copy numbers in a more highly expressed subcluster is particularly prevalent in teleosts. The differential expression and latent neofunctionalization of <it>vtg </it>genes in acanthomorph teleosts is an adaptive feature associated with oocyte hydration and spawning in the marine environment.</p

Insect glycerol transporters evolved by functional co-option and gene replacement

Transmembrane glycerol transport is typically facilitated by aquaglyceroporins in Prokaryota and Eukaryota. In holometabolan insects however, aquaglyceroporins are absent, yet several species possess polyol permeable aquaporins. It thus remains unknown how glycerol transport evolved in the Holometabola. By combining phylogenetic and functional studies, here we show that a more efficient form of glycerol transporter related to the water-selective channel AQP4 specifically evolved and multiplied in the insect lineage, resulting in the replacement of the ancestral branch of aquaglyceroporins in holometabolan insects. To recapitulate this evolutionary process, we generate specific mutants in distantly related insect aquaporins and human AQP4 and show that a single mutation in the selectivity filter converted a water-selective channel into a glycerol transporter at the root of the crown clade of hexapod insects. Integration of phanerozoic climate models suggests that these events were associated with the emergence of complete metamorphosis and the unparalleled radiation of insects.info:eu-repo/semantics/publishedVersio

Neurohypophysial and paracrine vasopressinergic signaling regulates aquaporin trafficking to hydrate marine teleost oocytes

The dual aquaporin (Aqp1ab1/Aqp1ab2)-mediated hydration of marine teleost eggs, which occurs during oocyte meiosis resumption (maturation), is considered a key adaptation underpinning their evolutionary success in the oceans. However, the endocrine signals controlling this mechanism are almost unknown. Here, we investigated whether the nonapeptides arginine vasopressin (Avp, formerly vasotocin) and oxytocin (Oxt, formerly isotocin) are involved in marine teleost oocyte hydration using the gilthead seabream (Sparus aurata) as a model. We show that concomitant with an increased systemic production of Avp and Oxt, the nonapeptides are also produced and accumulated locally in the ovarian follicles during oocyte maturation and hydration. Functional characterization of representative Avp and Oxt receptor subtypes indicates that Avpr1aa and Oxtrb, expressed in the postvitellogenic oocyte, activate phospholipase C and protein kinase C pathways, while Avpr2aa, which is highly expressed in the oocyte and in the follicular theca and granulosa cells, activates the cAMP-protein kinase A (PKA) cascade. Using ex vivo, in vitro and mutagenesis approaches, we determined that Avpr2aa plays a major role in the PKA-mediated phosphorylation of the aquaporin subdomains driving membrane insertion of Aqp1ab2 in the theca and granulosa cells, and of Aqp1ab1 and Aqp1ab2 in the distal and proximal regions of the oocyte microvilli, respectively. The data further indicate that luteinizing hormone, which surges during oocyte maturation, induces the synthesis of Avp in the granulosa cells via progestin production and the nuclear progestin receptor. Collectively, our data suggest that both the neurohypophysial and paracrine vasopressinergic systems integrate to differentially regulate the trafficking of the Aqp1ab-type paralogs via a common Avp-Avpr2aa-PKA pathway to avoid competitive occupancy of the same plasma membrane space and maximize water influx during oocyte hydration

The vertebrate Aqp14 water channel is a neuropeptide-regulated polytransporter

Water channels (aquaporins) were originally discovered in mammals with fourteen subfamilies now identified (AQP0-13). Here we show that a functional Aqp14 subfamily phylogenetically related to AQP4-type channels exists in all vertebrate lineages except hagfishes and eutherian mammals. In contrast to the water-selective classical aquaporins, which have four aromatic-arginine constriction residues, Aqp14 proteins present five non-aromatic constriction residues and facilitate the permeation of water, urea, ammonia, H2O2 and glycerol. Immunocytochemical assays suggest that Aqp14 channels play important osmoregulatory roles in piscine seawater adaptation. Our data indicate that Aqp14 intracellular trafficking is tightly regulated by the vasotocinergic/isotocinergic neuropeptide and receptor systems, whereby protein kinase C and A transduction pathways phosphorylate highly conserved C-terminal residues to control channel plasma membrane insertion. The neuropeptide regulation of Aqp14 channels thus predates the vasotocin/vasopressin regulation of AQP2-5-6 orthologs observed in tetrapods. These findings demonstrate that vertebrate Aqp14 channels represent an ancient subfamily of neuropeptide-regulated polytransporters.publishedVersio

Lineage-level divergence of copepod glycerol transporters and the emergence of isoform-specific trafficking regulation

Transmembrane conductance of small uncharged solutes such as glycerol typically occurs through aquaglyceroporins (Glps), which are commonly encoded by multiple genes in metazoan organisms. To date, however, little is known concerning the evolution of Glps in Crustacea or what forces might underly such apparent gene redundancy. Here, we show that Glp evolution in Crustacea is highly divergent, ranging from single copy genes in species of pedunculate barnacles, tadpole shrimps, isopods, amphipods and decapods to up to 10 copies in diplostracan water fleas although with monophyletic origins in each lineage. By contrast the evolution of Glps in Copepoda appears to be polyphyletic, with surprisingly high rates of gene duplication occurring in a genera- and species-specific manner. Based upon functional experiments on the Glps from a parasitic copepod (Lepeophtheirus salmonis), we show that such lineage-level gene duplication and splice variation is coupled with a high rate of neofunctionalization. In the case of L. salmonis, splice variation of a given gene resulted in tissue- or sex-specific expression of the channels, with each variant evolving unique sites for protein kinase C (PKC)- or protein kinase A (PKA)-regulation of intracellular membrane trafficking. The combined data sets thus reveal that mutations favouring a high fidelity control of intracellular trafficking regulation can be a selection force for the evolution and retention of multiple Glps in copepods.publishedVersio

Unravelling the complex duplication history of deuterostome glycerol transporters

Transmembrane glycerol transport is an ancient biophysical property that evolved in selected subfamilies of water channel (aquaporin) proteins. Here, we conducted broad level genome (>550) and transcriptome (>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 >800 million years old and thus form the novel basis for proposing a pandeuterostome glp gene nomenclature.info:eu-repo/semantics/publishedVersio

A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa

Article publicat sota una PNAS license: https://www.pnas.org/authors/fees-and-licenses#license-to-publishThe primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate H2O2 efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish (Danio rerio) and the Atlantic salmon (Salmo salar), in which spermatozoa are activated in freshwater, an intracellular Ca2+ -signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N-terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (Sparus aurata), in which spermatozoa activation occurs in seawater, a cross-talk between Ca2+ - and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection

A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa

The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate H2O2 efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish (Danio rerio) and the Atlantic salmon (Salmo salar), in which spermatozoa are activated in freshwater, an intracellular Ca2+-signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (Sparus aurata), in which spermatozoa activation occurs in seawater, a cross-talk between Ca2+- and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection.info:eu-repo/semantics/acceptedVersio

Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs

Aquaporin-mediated oocyte hydration is considered important for the evolution of pelagic eggs and the radiative success of marine teleosts. However, the molecular regulatory mechanisms controlling this vital process are not fully understood. Here, we analyzed >400 piscine genomes to uncover a previously unknown teleost-specific aquaporin-1 cluster (TSA1C) comprised of tandemly arranged aqp1aa-aqp1ab2-aqp1ab1 genes. Functional evolutionary analysis of the TSA1C reveals a ∼300-million-year history of downstream aqp1ab-type gene loss, neofunctionalization, and subfunctionalization, but with marine species that spawn highly hydrated pelagic eggs almost exclusively retaining at least one of the downstream paralogs. Unexpectedly, one-third of the modern marine euacanthomorph teleosts selectively retain both aqp1ab-type channels and co-evolved protein kinase-mediated phosphorylation sites in the intracellular subdomains together with teleost-specific Ywhaz-like (14-3-3ζ-like) binding proteins for co-operative membrane trafficking regulation. To understand the selective evolutionary advantages of these mechanisms, we show that a two-step regulated channel shunt avoids competitive occupancy of the same plasma membrane space in the oocyte and accelerates hydration. These data suggest that the evolution of the adaptive molecular regulatory features of the TSA1C facilitated the rise of pelagic eggs and their subsequent geodispersal in the oceanic currents.info:eu-repo/semantics/publishedVersio