RESUMO
Evolutionary perspectives on the deployment of immune factors following infection have been shaped by studies on a limited number of biomedical model systems with a heavy emphasis on vertebrate species. Although their contributions to contemporary immunology cannot be understated, a broader phylogenetic perspective is needed to understand the evolution of immune systems across Metazoa. In our study, we leverage differential gene expression analyses to identify genes implicated in the antiviral immune response of the acorn worm hemichordate, Saccoglossus kowalevskii, and place them in the context of immunity evolution within deuterostomes-the animal clade composed of chordates, hemichordates, and echinoderms. Following acute exposure to the synthetic viral double-stranded RNA analog, poly(I:C), we show that S. kowalevskii responds by regulating the transcription of genes associated with canonical innate immunity signaling pathways (e.g., nuclear factor κB and interferon regulatory factor signaling) and metabolic processes (e.g., lipid metabolism), as well as many genes without clear evidence of orthology with those of model species. Aggregated across all experimental time point contrasts, we identify 423 genes that are differentially expressed in response to poly(I:C). We also identify 147 genes with altered temporal patterns of expression in response to immune challenge. By characterizing the molecular toolkit involved in hemichordate antiviral immunity, our findings provide vital evolutionary context for understanding the origins of immune systems within Deuterostomia.
Assuntos
Cordados não Vertebrados , Cordados , Animais , Filogenia , Antivirais , Vertebrados , Equinodermos , Cordados não Vertebrados/genéticaRESUMO
Deuterostomes comprise three phyla with radically different body plans. Phylogenetic bracketing of the living deuterostome clades suggests the latest common ancestor of echinoderms, hemichordates and chordates was a bilaterally symmetrical worm with pharyngeal openings, with these characters lost in echinoderms. Early fossil echinoderms with pharyngeal openings have been described, but their interpretation is highly controversial. Here, we critically evaluate the evidence for pharyngeal structures (gill bars) in the extinct stylophoran echinoderms Lagynocystis pyramidalis and Jaekelocarpus oklahomensis using virtual models based on high-resolution X-ray tomography scans of three-dimensionally preserved fossil specimens. Multivariate analyses of the size, spacing and arrangement of the internal bars in these fossils indicate they are substantially more similar to gill bars in modern enteropneust hemichordates and cephalochordates than to other internal bar-like structures in fossil blastozoan echinoderms. The close similarity between the internal bars of the stylophorans L. pyramidalis and J. oklahomensis and the gill bars of extant chordates and hemichordates is strong evidence for their homology. Differences between these internal bars and bar-like elements of the respiratory systems in blastozoans suggest these structures might have arisen through parallel evolution across deuterostomes, perhaps underpinned by a common developmental genetic mechanism.
Assuntos
Cordados não Vertebrados , Cordados , Animais , Evolução Biológica , Cordados não Vertebrados/genética , Equinodermos , Fósseis , Brânquias , FilogeniaRESUMO
The Origin of Chordates has fascinated scientists from the time of Charles Darwin's publication "Descent of Man" in 1871. For over 100 years, it was accepted that chordates evolved from tunicates, our sessile invertebrate sister group. However, genomic and embryonic analyses have shown that lancelets have a body plan and genome much more like vertebrates than do tunicates. In 2000, we proposed a worm-like hypothesis of chordate origins, and genomic and embryonic studies in the past 20 years have supported this hypothesis. This hypothesis contends that the deuterostome ancestor was worm-like, with gill slits, very much like a chordate. In contrast, tunicates have a very derived adult body plan that evolved independently. Here, we review the current understanding of deuterostome phylogeny and supporting evidence for the relationships within each phylum. Then we discuss our hypothesis for chordate origins and evidence to support it. We explore some of the evolutionary changes that ascidians have made to their adult body plan and some of the key gene regulatory networks that have been elucidated in Ciona. Finally, we end with insights that we have gained from studying tailless ascidians for the past 30 years. We've found that differentiation genes, at the end of the gene regulatory networks, become pseudogenes and nonfunctional, even though they are still expressed in tailless ascidians. We expect that eventually these pseudogenes will not be expressed and the ascidian larval body plan is abandoned, leaving the embryo to develop directly into an adult.
Assuntos
Evolução Biológica , Urocordados , Vertebrados , Animais , Cordados não Vertebrados/genética , Ciona/genética , Embrião não Mamífero , Regulação da Expressão Gênica no Desenvolvimento , Redes Reguladoras de Genes , Filogenia , Pseudogenes , Urocordados/anatomia & histologia , Urocordados/embriologia , Urocordados/genéticaRESUMO
The trunk is a key feature of the bilaterian body plan. Despite spectacular morphological diversity in bilaterian trunk anatomies, most insights into trunk development are from segmented taxa, namely arthropods and chordates. Mechanisms of posterior axis elongation (PAE) and segmentation are tightly coupled in arthropods and vertebrates, making it challenging to differentiate between the underlying developmental mechanisms specific to each process. Investigating trunk elongation in unsegmented animals facilitates examination of mechanisms specific to PAE and provides a different perspective for testing hypotheses of bilaterian trunk evolution. Here we investigate the developmental roles of canonical Wnt and Notch signaling in the hemichordate Saccoglossus kowalevskii and reveal that both pathways play key roles in PAE immediately following the completion of gastrulation. Furthermore, our functional analysis of the role of Brachyury is supportive of a Wnt-Brachyury feedback loop during PAE in S. kowalevskii, establishing this key regulatory interaction as an ancestral feature of deuterostomes. Together, our results provide valuable data for testing hypotheses of bilaterian trunk evolution.
Assuntos
Padronização Corporal , Cordados não Vertebrados , Regulação da Expressão Gênica no Desenvolvimento , Animais , Padronização Corporal/genética , Padronização Corporal/fisiologia , Cordados não Vertebrados/embriologia , Cordados não Vertebrados/genética , Cordados não Vertebrados/crescimento & desenvolvimento , Cordados não Vertebrados/fisiologia , Embrião não Mamífero/embriologia , Embrião não Mamífero/fisiologia , Desenvolvimento Embrionário/genética , Desenvolvimento Embrionário/fisiologia , Regulação da Expressão Gênica no Desenvolvimento/genética , Regulação da Expressão Gênica no Desenvolvimento/fisiologia , Receptores Notch/genética , Receptores Notch/fisiologia , Via de Sinalização Wnt/genética , Via de Sinalização Wnt/fisiologiaRESUMO
Previously, we demonstrated that the animal aspartate racemase (AspR) gene has evolved from the serine racemase (SerR) gene by acquisition of three consecutive serine residues (Ser155-Ser156-Ser157) involved in the strong AspR activity, and this event has occurred independently and frequently during animal evolution. In the present study, we cloned and characterized two mammalian SerR homologous genes from the hemichordate acorn worm (Saccoglossus kowalevskii). The enzymes have been identified as an AspR and an aspartate/glutamate racemase (Asp/GluR) on the basis of their kinetic parameters. The S. kowalevskii Asp/GluR shows comparable substrate affinity and high catalytic efficiency (kcat/Km) for both aspartate and glutamate and is the first reported enzyme from animals that can synthesize d-glutamate. Amino acid sequence alignment analysis and site-directed mutagenesis studies have revealed that the amino acid residue at position 156, which is serine in AspR and alanine in Asp/GluR, is associated with binding and recognition of glutamate and aspartate. Phylogenetic analysis suggests that the S. kowalevskii AspR gene has evolved from the SerR gene after the divergence of hemichordata and vertebrate lineages by acquisition of the three serine residues at position 155 to 157 as in the case of other animal AspR genes. Furthermore, the S. kowalevskii Asp/GluR gene is the result of AspR gene duplication and several amino acid substitutions including that of the 156th serine residue with alanine. The fact that SerR has acquired substrate specificity towards aspartate or glutamate raises the possibility that synthesis of other d-amino acids is carried out by enzymes evolved from SerR.
Assuntos
Isomerases de Aminoácido , Cordados não Vertebrados , Filogenia , Isomerases de Aminoácido/genética , Isomerases de Aminoácido/metabolismo , Sequência de Aminoácidos , Animais , Ácido Aspártico/economia , Ácido Aspártico/metabolismo , Cordados não Vertebrados/enzimologia , Cordados não Vertebrados/genética , Clonagem MolecularRESUMO
Hemichordates are a phylum of marine invertebrate deuterostomes that are closely related to chordates, and represent one of the most promising models to provide insights into early deuterostome evolution. The genome of the hemichordate, Saccoglossus kowalevskii, reveals an extensive set of non-coding elements conserved across all three deuterostome phyla. Functional characterization and cross-phyla comparisons of these putative regulatory elements will enable a better understanding of enhancer evolution, and subsequently how changes in gene regulation give rise to morphological innovation. Here, we describe an efficient method of transgenesis for the characterization of non-coding elements in S. kowalevskii. We first test the capacity of an I-SceI transgenesis system to drive ubiquitous or regionalized gene expression, and to label specific cell types. Finally, we identified a minimal promoter that can be used to test the capacity of putative enhancers in S. kowalevskii. This work demonstrates that this I-SceI transgenesis technique, when coupled with an understanding of chromatin accessibility, can be a powerful tool for studying how evolutionary changes in gene regulatory mechanisms contributed to the diversification of body plans in deuterostomes.
Assuntos
Animais Geneticamente Modificados/genética , Técnicas de Transferência de Genes/instrumentação , Poliquetos/genética , Animais , Evolução Biológica , Cordados/genética , Cordados não Vertebrados/genética , Evolução Molecular , Técnicas de Transferência de Genes/veterinária , Genoma , InvertebradosRESUMO
Many animals are indirect developers with distinct larval and adult body plans [1]. The molecular basis of differences between larval and adult forms is often poorly understood, adding a level of uncertainty to comparative developmental studies that use data from both indirect and direct developers. Here we compare the larval and adult body plans of an indirect developing hemichordate, Schizocardium californicum [2]. We describe the expression of 27 transcription factors with conserved roles in deuterostome ectodermal anteroposterior (AP) patterning in developing embryos, tornaria larvae, and post-metamorphic juveniles and show that the tornaria larva of S. californicum is transcriptionally similar to a truncated version of the adult. The larval ectoderm has an anterior molecular signature, while most of the trunk, defined by the expression of hox1-7, is absent. Posterior ectodermal activation of Hox is initiated in the late larva prior to metamorphosis, in preparation for the transition to the adult form, in which the AP axis converges on a molecular architecture similar to that of the direct developing hemichordate Saccoglossus kowalevskii. These results identify a molecular correlate of a major difference in body plan between hemichordate larval and adult forms and confirm the hypothesis that deuterostome larvae are "swimming heads" [3]. This will allow future comparative studies with hemichordates to take into account molecular differences caused by early life history evolution within the phylum. Additionally, comparisons with other phyla suggest that a delay in trunk development is a feature of indirect development shared across distantly related phyla.
Assuntos
Cordados não Vertebrados/crescimento & desenvolvimento , Regulação da Expressão Gênica no Desenvolvimento , Genes Homeobox , Morfogênese , Animais , Evolução Biológica , Padronização Corporal , Cordados não Vertebrados/genética , Larva/genética , Fatores de Transcrição/genética , Fatores de Transcrição/metabolismoRESUMO
Phylum Hemichordata, composed of worm-like Enteropneusta and colonial Pterobranchia, has been reported to only contain about 100 species. However, recent studies of hemichordate phylogeny and taxonomy suggest the species number has been largely underestimated. One issue is that species must be described by experts, and historically few taxonomists have studied this group of marine invertebrates. Despite this previous lack of coverage, interest in hemichordates has piqued in the past couple of decades, as they are critical to understanding the evolution of chordates-as acorn worms likely resemble the deuterostome ancestor more closely than any other extant animal. This review provides an overview of our current knowledge of hemichordates, focusing specifically on their global biodiversity, geographic distribution, and taxonomy. Using information available in the World Register of Marine Species and published literature, we assembled a list of 130 described, extant species. The majority (83%) of these species are enteropneusts, and more taxonomic descriptions are forthcoming. Ptychoderidae contained the greatest number of species (41 species), closely followed by Harrimaniidae (40 species), of the recognized hemichordate families. Hemichordates are found throughout the world's oceans, with the highest reported numbers by regions with marine labs and diligent taxonomic efforts (e.g. North Pacific and North Atlantic). Pterobranchs are abundant in Antarctica, but have also been found at lower latitudes. We consider this a baseline report and expect new species of Hemichordata will continue to be discovered and described as new marine habitats are characterized and explored.
Assuntos
Biodiversidade , Cordados não Vertebrados , Animais , Organismos Aquáticos , Cordados não Vertebrados/anatomia & histologia , Cordados não Vertebrados/classificação , Cordados não Vertebrados/genética , Geografia , FilogeniaRESUMO
Paramyosin is a myosin-binding protein characteristic of invertebrate animals, while troponin is a Ca2+-dependent regulator of muscle contraction. Both proteins are widely distributed in protostomes, while in deuterostomes, their distribution is limited; namely, presence of paramyosin and absence of troponin are common features in echinoderm muscles, while muscles of chordates contain troponin but lack paramyosin. In this study, we examined the muscle of a hemichordate, acorn worm, to clarify whether this animal is like echinoderms or like the other deuterostome animals. We found a 100-kDa protein in the smooth muscle of acorn worm. This protein was identified with paramyosin, since the purified protein formed paracrystals with a constant axial periodicity in the presence of divalent cations as paramyosin of other animals, showed ability to interact with myosin and shared common antigenicity with echinoderm paramyosin. On the other hand, troponin band was not detected in isolated thin filaments, and the filaments increased myosin-ATPase activity in a Ca2+-independent manner. The results indicate that troponin is lacking in thin filaments of acorn worm muscle just as in those of echinoderms. The muscle of hemichordate acorn worm is quite similar to echinoderm muscles, but different from chordate muscles.
Assuntos
Cordados não Vertebrados , Músculo Liso/metabolismo , Tropomiosina , Animais , Cordados não Vertebrados/genética , Cordados não Vertebrados/metabolismo , Tropomiosina/genética , Tropomiosina/metabolismoRESUMO
Acorn worms, also known as enteropneust (literally, 'gut-breathing') hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal 'gill' slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.
Assuntos
Cordados não Vertebrados/genética , Evolução Molecular , Genoma/genética , Animais , Cordados não Vertebrados/classificação , Sequência Conservada/genética , Equinodermos/classificação , Equinodermos/genética , Família Multigênica/genética , Filogenia , Transdução de Sinais , Sintenia/genética , Fator de Crescimento Transformador betaRESUMO
Opsins--G-protein coupled receptors involved in photoreception--have been extensively studied in the animal kingdom. The present work provides new insights into opsin-based photoreception and photoreceptor cell evolution with a first analysis of opsin sequence data for a major deuterostome clade, the Ambulacraria. Systematic data analysis, including for the first time hemichordate opsin sequences and an expanded echinoderm dataset, led to a robust opsin phylogeny for this cornerstone superphylum. Multiple genomic and transcriptomic resources were surveyed to cover each class of Hemichordata and Echinodermata. In total, 119 ambulacrarian opsin sequences were found, 22 new sequences in hemichordates and 97 in echinoderms (including 67 new sequences). We framed the ambulacrarian opsin repertoire within eumetazoan diversity by including selected reference opsins from non-ambulacrarians. Our findings corroborate the presence of all major ancestral bilaterian opsin groups in Ambulacraria. Furthermore, we identified two opsin groups specific to echinoderms. In conclusion, a molecular phylogenetic framework for investigating light-perception and photobiological behaviors in marine deuterostomes has been obtained.
Assuntos
Cordados não Vertebrados/genética , Equinodermos/genética , Evolução Molecular , Opsinas/metabolismo , Filogenia , Sequência de Aminoácidos , Animais , Regulação da Expressão Gênica , Modelos Moleculares , Dados de Sequência Molecular , Opsinas/genética , Conformação ProteicaRESUMO
Fibroblast growth factors (FGFs) are a group of ligands that play multiple roles during development by transducing signals through FGF receptors (FGFRs) to downstream factors. At least 22 FGF ligands and 4 receptors have been identified in vertebrates, while six to eight FGF ligands and a single FGFR are present in invertebrate chordates, such as tunicates and amphioxus. The chordate FGFs can be categorized into at least seven subfamilies, and the members of which expanded during the evolution of early vertebrates. In contrast, only one FGF and two FGFRs have been found in sea urchins. Thus, it is unclear whether the FGF subfamilies duplicated in the lineage leading to the chordates, or sea urchins lost several fgf genes. Analyses of the FGF signaling repertoire in hemichordates, which together with echinoderms form the closest group to the chordates, may provide insights into the evolution of FGF signaling in deuterostomes. In this study, we identified five FGFs and three FGFRs from Ptychodera flava, an indirect-developing hemichordate acorn worm. Phylogenetic analyses revealed that hemichordates possess a conserved FGF8/17/18 in addition to several putative hemichordate-specific FGFs. Analyses of sequence similarity and protein domain organizations suggested that the sea urchin and hemichordate FGFRs arose from independent lineage-specific duplications. Furthermore, the acorn worm fgf and fgfr genes were demonstrated to be expressed during P. flava embryogenesis. These results set the foundations for further functional studies of FGF signaling in hemichordates and provided insights into the evolutionary history of the FGF repertoire.
Assuntos
Cordados não Vertebrados/metabolismo , Fatores de Crescimento de Fibroblastos/metabolismo , Regulação da Expressão Gênica no Desenvolvimento/fisiologia , Sequência de Aminoácidos , Animais , Cordados não Vertebrados/genética , Fatores de Crescimento de Fibroblastos/genética , Dados de Sequência Molecular , Filogenia , Receptores de Fatores de Crescimento de Fibroblastos/genética , Receptores de Fatores de Crescimento de Fibroblastos/metabolismo , Transdução de SinaisRESUMO
Seven nuclear and mitochondrial DNA markers were examined in 12 specimens of Ptychodera flava, a model acorn worm used in molecular biology, collected in Japan from three local populations with different modes of living. A comparison of intraspecific results did not show genetically isolated populations despite the species' enclave habitats and asexual reproduction. Moreover, both the nuclear 18S ribosomal RNA gene and mitochondrial 16S ribosomal RNA gene sequences were identical to those from Moorea in French Polynesia, nearly 10,000 kilometers away from Japan. I also provide the first definitive information regarding polymorphisms in 18S ribosomal RNA gene, the external transcribed spacer (ETS), internal transcribed spacers (ITS), and mitochondrial cytochrome c oxidase subunit 1 (mtCO1) sequence in hemichordates using newly designed primer sets, and I show both high larval vagility and certain criteria for the molecular identification of this species.
Assuntos
Cordados não Vertebrados/genética , Polimorfismo Genético , RNA Ribossômico 18S/genética , Animais , DNA Espaçador Ribossômico/genética , FilogeniaRESUMO
Ambulacraria, comprising Hemichordata and Echinodermata, is closely related to Chordata, making it integral to understanding chordate origins and polarizing chordate molecular and morphological characters. Unfortunately, relationships within Hemichordata and Echinodermata have remained unresolved, compromising our ability to extrapolate findings from the most closely related molecular and developmental models outside of Chordata (e.g., the acorn worms Saccoglossus kowalevskii and Ptychodera flava and the sea urchin Strongylocentrotus purpuratus). To resolve long-standing phylogenetic issues within Ambulacraria, we sequenced transcriptomes for 14 hemichordates as well as 8 echinoderms and complemented these with existing data for a total of 33 ambulacrarian operational taxonomic units (OTUs). Examination of leaf stability values revealed rhabdopleurid pterobranchs and the enteropneust Stereobalanus canadensis were unstable in placement; therefore, analyses were also run without these taxa. Analyses of 185 genes resulted in reciprocal monophyly of Enteropneusta and Pterobranchia, placed the deep-sea family Torquaratoridae within Ptychoderidae, and confirmed the position of ophiuroid brittle stars as sister to asteroid sea stars (the Asterozoa hypothesis). These results are consistent with earlier perspectives concerning plesiomorphies of Ambulacraria, including pharyngeal gill slits, a single axocoel, and paired hydrocoels and somatocoels. The resolved ambulacrarian phylogeny will help clarify the early evolution of chordate characteristics and has implications for our understanding of major fossil groups, including graptolites and somasteroideans.
Assuntos
Cordados não Vertebrados/genética , Filogenia , Animais , Evolução Biológica , Cordados/classificação , Cordados/genética , Cordados não Vertebrados/classificação , Funções Verossimilhança , TranscriptomaRESUMO
Tandem simple sequence repeats (SSRs) are one of the most popular molecular markers in genetic analysis owing to their ubiquitous occurrence,high reproducibility, multiallelic nature, and codominant mode. High mutability makes SSRs play a role in genome evolution and correspondingly show different patterns. Comparative analysis of genomic SSRs in different taxonomic groups usually focuses on land species, while marine animals have been neglected. This study examined the abundance of genomic SSRs with repeated unit lengths of 1-6 bp in 30 marine animals including nine taxonomic groups and further compared with the land species. More than thousands of SSRs were discovered in every organism which provided a huge resource for the development of molecular markers. Thirty marine animals showed profound differences in SSR characteristics, but some group-specific trends were also found. Both similarities and differences of repeat patterns were discovered between the land and marine species. Two taxon-specific SSR types were discovered: the pentanucleotides motif AGAGG in Euteleostei and the hexanucleotide repeats of ATGTAC in Porifera and Echinodermata. Gene ontology (GO) enrichment analysis of two representative species (Amphimedon queenslandica for Porifera and Strongylocentrotus purpuratus for Echinodermata) revealed functional preference of the ATGTAC motif associated genes, and this might hint at evolutionary significance.
Assuntos
Cordados não Vertebrados/genética , Peixes/genética , Marcadores Genéticos/genética , Variação Genética , Invertebrados/genética , Biologia Marinha/métodos , Repetições de Microssatélites/genética , Animais , Ontologia Genética , Tamanho do Genoma/genética , Genômica/métodos , Especificidade da EspécieRESUMO
A single specimen of a previously undescribed acorn worm in the family Torquaratoridae was trawled from a bottom depth of about 350 m in the Kara Sea (Russian Arctic). The new species is the shallowest of the exclusively deep-sea torquaratorids found to date, possibly an example of high-latitude emergence. On the basis of ribosomal DNA sequences and morphology, the worm is described here as the holotype of Coleodesmium karaensis n. gen., n. sp. It is most similar in overall body shape to the previously described enteropneust genus Allapasus, but is uniquely characterized by a tubular component of the proboscis skeleton ensheathing the collar nerve cord. Additionally, within the proboscis, the sparseness of the musculature of C. karaensis clearly distinguishes it from the much more muscular members of Allapasus. The holotype is a female bearing about a dozen embryos on the surface of her pharyngeal region, each recessed within a shallow depression in the dorsal epidermis. The embryos, ranging from late gastrula to an early stage of coelom formation, are a little more than 1 mm in diameter and surrounded by a thin membrane. Each embryo comprises an external ectoderm of monociliated cells (not arranged in obvious ciliated bands) and an internal endo-mesoderm; the blastopore is closed. In the most advanced embryos, the anterior coelom is starting to constrict off from the archenteron. Coleodesmium karaensis is the first enteropneust (and indeed the first hemichordate) found brooding embryos on the surface of the mother's body.
Assuntos
Cordados não Vertebrados/classificação , Cordados não Vertebrados/fisiologia , Animais , Regiões Árticas , Cordados não Vertebrados/genética , Cordados não Vertebrados/ultraestrutura , Feminino , Microscopia Eletrônica de Varredura , Dados de Sequência Molecular , Filogenia , RNA Ribossômico 16S/genética , RNA Ribossômico 18S/genética , Reprodução , Federação Russa , Especificidade da EspécieRESUMO
Acorn worms, or enteropneusts, are vermiform hemichordates that occupy an important position in deuterostome phylogeny. Allied to pterobranch hemichordates, small colonial tube dwellers, modern enteropneusts were thought to be tubeless. However, understanding of hemichordate diversity is poor, as evidenced by absence of reports from some oceanic regions and recent descriptions of large epibenthic deep-water enteropneusts, Torquaratoridae. Here we show, based on expeditions to Antarctica, that some acorn worms produce conspicuous tubes that persist for days. Interestingly, recent fossil descriptions show a Middle Cambrian acorn worm lived in tubes, leading to speculation that these fossils may have been pterobranch forbearers. Our discovery provides the alternative interpretation that these fossils are similar to modern-day torquaratorids and that some behaviours have been conserved for over 500 million years. Moreover, the frequency of Antarctic enteropneusts observed attests to our limited knowledge of Antarctic marine ecosystems, and strengthens hypotheses relating more northern deep-sea fauna to Antarctic shelf fauna.
Assuntos
Comportamento Animal/fisiologia , Cordados não Vertebrados/fisiologia , Animais , Regiões Antárticas , Cordados não Vertebrados/genética , Fósseis , Oceanos e Mares , FilogeniaRESUMO
BACKGROUND: ParaHox and Hox genes are thought to have evolved from a common ancestral ProtoHox cluster or from tandem duplication prior to the divergence of cnidarians and bilaterians. Similar to Hox clusters, chordate ParaHox genes including Gsx, Xlox, and Cdx, are clustered and their expression exhibits temporal and spatial colinearity. In non-chordate animals, however, studies on the genomic organization of ParaHox genes are limited to only a few animal taxa. Hemichordates, such as the Enteropneust acorn worms, have been used to gain insights into the origins of chordate characters. In this study, we investigated the genomic organization and expression of ParaHox genes in the indirect developing hemichordate acorn worm Ptychodera flava. RESULTS: We found that P. flava contains an intact ParaHox cluster with a similar arrangement to that of chordates. The temporal expression order of the P. flava ParaHox genes is the same as that of the chordate ParaHox genes. During embryogenesis, the spatial expression pattern of PfCdx in the posterior endoderm represents a conserved feature similar to the expression of its orthologs in other animals. On the other hand, PfXlox and PfGsx show a novel expression pattern in the blastopore. Nevertheless, during metamorphosis, PfXlox and PfCdx are expressed in the endoderm in a spatially staggered pattern similar to the situation in chordates. CONCLUSIONS: Our study shows that P. flava ParaHox genes, despite forming an intact cluster, exhibit temporal colinearity but lose spatial colinearity during embryogenesis. During metamorphosis, partial spatial colinearity is retained in the transforming larva. These results strongly suggest that intact ParaHox gene clustering was retained in the deuterostome ancestor and is correlated with temporal colinearity.
Assuntos
Cordados não Vertebrados/genética , Evolução Molecular , Proteínas de Homeodomínio/genética , Família Multigênica , Animais , Cordados não Vertebrados/classificação , Genoma , FilogeniaRESUMO
Saccoglossus kowalevskii (the acorn worm) is a hemichordate belonging to the superphylum of deuterostome bilateral animals. Hemichordates are sister group to echinoderms, and closely related to chordates. S. kowalevskii has chordate like morphological traits and serves as an important model organism, helping developmental biologists to understand the evolution of the central nervous system (CNS). Despite being such an important model organism, the signalling system repertoire of the largest family of integral transmembrane receptor proteins, G protein-coupled receptors (GPCRs) is largely unknown in S. kowalevskii. Here, we identified 260 unique GPCRs and classified as many as 257 of them into five main mammalian GPCR families; Glutamate (23), Rhodopsin (212), Adhesion (18), Frizzled (3) and Secretin (1). Despite having a diffuse nervous system, the acorn worm contains well conserved orthologues for human Adhesion and Glutamate family members, with a similar N-terminal domain architecture. This is particularly true for genes involved in CNS development and regulation in vertebrates. The average sequence identity between the GPCR orthologues in human and S. kowalevskii is around 47%, and this is same as observed in couple of the closest vertebrate relatives, Ciona intestinalis (41%) and Branchiostoma floridae (~47%). The Rhodopsin family has fewer members than vertebrates and lacks clear homologues for 6 of the 13 subgroups, including olfactory, chemokine, prostaglandin, purine, melanocyte concentrating hormone receptors and MAS-related receptors. However, the peptide and somatostatin binding receptors have expanded locally in the acorn worm. Overall, this study is the first large scale analysis of a major signalling gene superfamily in the hemichordate lineage. The establishment of orthologue relationships with genes involved in neurotransmission and development of the CNS in vertebrates provides a foundation for understanding the evolution of signal transduction and allows for further investigation of the hemichordate neurobiology.