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Genome Biology and Evolution Oct 2022Fox genes are a large and conserved family of transcription factors involved in many key biological processes, including embryogenesis and body patterning. Although the...
Fox genes are a large and conserved family of transcription factors involved in many key biological processes, including embryogenesis and body patterning. Although the role of Fox genes has been studied in an array of model systems, comprehensive comparative studies in Spiralia-a large clade of invertebrate animals including molluscs and annelids-are scarce but much needed to better understand the evolutionary history of this gene family. Here, we reconstruct and functionally characterize the Fox gene complement in the annelid Owenia fusiformis, a slow evolving species and member of the sister group to all remaining annelids. The genome of O. fusiformis contains at least a single ortholog for 20 of the 22 Fox gene classes that are ancestral to Bilateria, including an ortholog of the recently discovered foxT class. Temporal and spatial expression dynamics reveal a conserved role of Fox genes in gut formation, mesoderm patterning, and apical organ and cilia formation in Annelida and Spiralia. Moreover, we uncover an ancestral expansion of foxQ2 genes in Spiralia, represented by 11 paralogs in O. fusiformis. Notably, although all foxQ2 copies have apical expression in O. fusiformis, they show variable spatial domains and staggered temporal activation, which suggest cooperation and sub-functionalization among foxQ2 genes for the development of apical fates in this annelid. Altogether, our study informs the evolution and developmental roles of Fox genes in Annelida and Spiralia generally, providing the basis to explore how regulatory changes in Fox gene expression might have contributed to developmental and morphological diversification in Spiralia.
Topics: Animals; Annelida; Body Patterning; Invertebrates; Phylogeny; Polychaeta; Transcription Factors
PubMed: 36099507
DOI: 10.1093/gbe/evac139 -
Parasite (Paris, France) Sep 2008Annelids have had a long history in comparative embryology and morphology, which has helped to establish them in zoology textbooks as an ideal system to understand the... (Review)
Review
Annelids have had a long history in comparative embryology and morphology, which has helped to establish them in zoology textbooks as an ideal system to understand the evolution of the typical triploblastic, coelomate, protostome condition. In recent years there has been a relative upsurge in embryological data, particularly with regard to the expression and function of developmental control genes. Polychaetes, as well as other annelids such as the parasitic leech, are now also entering the age of comparative genomics. All of this comparative data has had an important impact on our views of the ancestral conditions at various levels of the animal phylogeny, including the bilaterian ancestor and the nature of the annelid ancestor. Here we review some of the recent advances made in annelid comparative development and genomics, revealing a hitherto unsuspected level of complexity in these ancestors. It is also apparent that the transition to a parasitic lifestyle leads to, or requires, extensive modifications and derivations at both the genomic and embryological levels.
Topics: Animals; Annelida; Biological Evolution; Developmental Biology; Genomics
PubMed: 18814702
DOI: 10.1051/parasite/2008153321 -
Philosophical Transactions of the Royal... Feb 2010It is proposed here that a biphasic life cycle with partial dedifferentiation of intermediate juvenile or larval stages represents the mainstream developmental mode of... (Review)
Review
It is proposed here that a biphasic life cycle with partial dedifferentiation of intermediate juvenile or larval stages represents the mainstream developmental mode of metazoans. Developmental plasticity of differentiated cells is considered the essential characteristic of indirect development, rather than the exclusive development of the adult from 'set-aside' cells. Many differentiated larval cells of indirect developers resume proliferation, partially dedifferentiate and contribute to adult tissues. Transcriptional pluripotency of differentiated states has premetazoan origins and seems to be facilitated by histone variant H2A.Z. Developmental plasticity of differentiated states also facilitates the evolution of polyphenism. Uncertainty remains about whether the most recent common ancestor of protostomes and deuterostomes was a direct or an indirect developer, and how the feeding larvae of bilaterians are related to non-feeding larvae of sponges and cnidarians. Feeding ciliated larvae of bilaterians form their primary gut opening by invagination, which seems related to invagination in cnidarians. Formation of the secondary gut opening proceeds by protostomy or deuterostomy, and gene usage suggests serial homology of the mouth and anus. Indirect developers do not use the Hox vector to build their ciliated larvae, but the Hox vector is associated with the construction of the reproductive portion of the animal during feeding-dependent posterior growth. It is further proposed that the original function of the Hox cluster was in gonad formation rather than in anteroposterior diversification.
Topics: Animals; Annelida; Biological Evolution; Cell Differentiation; Cell Transdifferentiation; Gastrulation; Gene Expression Regulation, Developmental; Gene Regulatory Networks; Genes, Homeobox; Genitalia; Growth and Development; Larva; Life Cycle Stages; Models, Biological; Phylogeny; Stem Cells
PubMed: 20083640
DOI: 10.1098/rstb.2009.0253 -
ELife Dec 2022Cells form networks in animal tissues through synaptic, chemical, and adhesive links. Invertebrate muscle cells often connect to other cells through desmosomes, adhesive...
Cells form networks in animal tissues through synaptic, chemical, and adhesive links. Invertebrate muscle cells often connect to other cells through desmosomes, adhesive junctions anchored by intermediate filaments. To study desmosomal networks, we skeletonised 853 muscle cells and their desmosomal partners in volume electron microscopy data covering an entire larva of the annelid . Muscle cells adhere to each other, to epithelial, glial, ciliated, and bristle-producing cells and to the basal lamina, forming a desmosomal connectome of over 2000 cells. The aciculae - chitin rods that form an endoskeleton in the segmental appendages - are highly connected hubs in this network. This agrees with the many degrees of freedom of their movement, as revealed by video microscopy. Mapping motoneuron synapses to the desmosomal connectome allowed us to infer the extent of tissue influenced by motoneurons. Our work shows how cellular-level maps of synaptic and adherent force networks can elucidate body mechanics.
Topics: Animals; Connectome; Larva; Annelida; Polychaeta; Muscles
PubMed: 36537659
DOI: 10.7554/eLife.71231 -
EMBO Reports Dec 2002Neuroglobin and cytoglobin are two recently discovered members of the vertebrate globin family. Both are intracellular proteins endowed with hexacoordinated heme-Fe... (Review)
Review
Neuroglobin and cytoglobin are two recently discovered members of the vertebrate globin family. Both are intracellular proteins endowed with hexacoordinated heme-Fe atoms, in their ferrous and ferric forms, and display O2 affinities comparable with that of myoglobin. Neuroglobin, which is predominantly expressed in nerve cells, is thought to protect neurons from hypoxic-ischemic injury. It is of ancient evolutionary origin, and is homologous to nerve globins of invertebrates. Cytoglobin is expressed in many different tissues, although at varying levels. It shares common ancestry with myoglobin, and can be traced to early vertebrate evolution. The physiological roles of neuroglobin and cytoglobin are not completely understood. Although supplying cells with O2 is the likely function, it is also possible that both globins act as O2-consuming enzymes or as O2 sensors. Here, we review what is currently known about neuroglobin and cytoglobin in terms of their function, tissue distribution and relatedness to the well-known hemoglobin and myoglobin. Strikingly, the data reveal that O2 metabolism in cells is more complicated than was thought before, requiring unexpected O2-binding proteins with potentially novel functional features.
Topics: Amino Acid Sequence; Animals; Annelida; Brain; Brain Chemistry; Conserved Sequence; Cytoglobin; Globins; Heme; Humans; Mice; Molecular Sequence Data; Nerve Tissue Proteins; Neuroglobin; Oxygen; Sequence Alignment; Zebrafish
PubMed: 12475928
DOI: 10.1093/embo-reports/kvf248 -
Current Biology : CB Nov 2008
Topics: Animals; Annelida; Biological Evolution; Body Patterning; Chordata; Drosophila
PubMed: 19000806
DOI: 10.1016/j.cub.2008.08.029 -
Pharmacology Research & Perspectives Oct 2021Pharmacology graduates require an understanding of both in vitro and in vivo drug responses but there has been a decline in animal use in pharmacology education over the...
Pharmacology graduates require an understanding of both in vitro and in vivo drug responses but there has been a decline in animal use in pharmacology education over the last 30 years. To address this, we present the novel invertebrate model, Lumbriculus variegatus, for in vivo testing of drugs in a teaching environment. We have developed two novel behavioral assays: the stereotypical movement assay, which measures the effect of drugs on the ability of L. variegatus to perform stereotypical movements following tactile stimulation, and the free locomotion assay, which measures drug effects on unstimulated movement. We report the effects of compounds with diverse pharmacodynamic properties on L. variegatus using these assays. The ryanodine receptor antagonist, dantrolene, altered the unstimulated movement of L. variegatus at 5 μM, whereas stimulated movement was inhibited at ≥25 μM. Lidocaine, a voltage-gated sodium channel blocker, and quinine, a nonselective sodium and potassium channel blocker, reduced both stimulated and unstimulated L. variegatus movement at ≥0.5 mM. Inhibitory effects of quinine persisted for up to 24 h after drug removal, whereas lidocaine effects were reduced 10 min after drug removal. Herein, we provide proof-of-concept utilization of L. variegatus as an organism for use in in vivo pharmacology education but without regulatory constraints or the need for specialized equipment and training.
Topics: Animals; Annelida; Behavior, Animal; Calcium Channel Blockers; Dantrolene; Lidocaine; Models, Animal; Movement; Muscle Relaxants, Central; Pharmacology; Quinine; Voltage-Gated Sodium Channel Blockers
PubMed: 34415088
DOI: 10.1002/prp2.853 -
BMC Genomics Mar 2009There are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. Although...
BACKGROUND
There are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. Although over one thousand metazoan genomes have been sequenced, the taxonomic sampling is highly biased, left with many phyla without a single representative of complete mitochondrial genome. Sipuncula (peanut worms or star worms) is a small taxon of worm-like marine organisms with an uncertain phylogenetic position. In this report, we present the mitochondrial genome sequence of Phascolosoma esculenta, the first complete mitochondrial genome of the phylum.
RESULTS
The mitochondrial genome of P.esculenta is 15,494 bp in length. The coding strand consists of 32.1% A, 21.5% C, 13.0% G, and 33.4% T bases (AT = 65.5%; AT skew = -0.019; GC skew = -0.248). It contains thirteen protein-coding genes (PCGs) with 3,709 codons in total, twenty-two transfer RNA genes, two ribosomal RNA genes and a non-coding AT-rich region (AT = 74.2%). All of the 37 identified genes are transcribed from the same DNA strand. Compared with the typical set of metazoan mt genomes, sipunculid lacks trnR but has an additional trnM. Maximum Likelihood and Bayesian analyses of the protein sequences show that Myzostomida, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group, which supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups.
CONCLUSION
This is the first report of a complete mitochondrial genome as a representative within the phylum Sipuncula. It shares many more similar features with the four known annelid and one echiuran mtDNAs. Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans). Hence annelid "key-characters" including segmentation may be more labile than previously assumed.
Topics: Animals; Annelida; Base Composition; DNA, Mitochondrial; Evolution, Molecular; Gene Order; Genes, rRNA; Genome, Mitochondrial; Nucleic Acid Conformation; Phylogeny; RNA, Transfer; Sequence Analysis, DNA
PubMed: 19327168
DOI: 10.1186/1471-2164-10-136 -
The International Journal of... 2014Animals differ markedly in their ability to regenerate, yet still little is known about how regeneration evolves. In recent years, important advances have been made in... (Review)
Review
Animals differ markedly in their ability to regenerate, yet still little is known about how regeneration evolves. In recent years, important advances have been made in our understanding of animal phylogeny and these provide new insights into the phylogenetic distribution of regeneration. The developmental basis of regeneration is also being investigated in an increasing number of groups, allowing commonalities and differences across groups to become evident. Here, we focus on regeneration in the Spiralia, a group that includes several champions of animal regeneration, as well as many groups with more limited abilities. We review the phylogenetic distribution and developmental processes of regeneration in four major spiralian groups: annelids, nemerteans, platyhelminths, and molluscs. Although comparative data are still limited, this review highlights phylogenetic and developmental patterns that are emerging regarding regeneration in spiralians and identifies important avenues for future research.
Topics: Animals; Annelida; Biological Evolution; Mollusca; Phylogeny; Platyhelminths; Regeneration
PubMed: 25690976
DOI: 10.1387/ijdb.140142ab -
Communications Biology Jan 2021Earthworms (Annelida: Crassiclitellata) are widely distributed around the world due to their ancient origination as well as adaptation and invasion after introduction...
Earthworms (Annelida: Crassiclitellata) are widely distributed around the world due to their ancient origination as well as adaptation and invasion after introduction into new habitats over the past few centuries. Herein, we report a 1.2 Gb complete genome assembly of the earthworm Amynthas corticis based on a strategy combining third-generation long-read sequencing and Hi-C mapping. A total of 29,256 protein-coding genes are annotated in this genome. Analysis of resequencing data indicates that this earthworm is a triploid species. Furthermore, gene family evolution analysis shows that comprehensive expansion of gene families in the Amynthas corticis genome has produced more defensive functions compared with other species in Annelida. Quantitative proteomic iTRAQ analysis shows that expression of 147 proteins changed in the body of Amynthas corticis and 16 S rDNA sequencing shows that abundance of 28 microorganisms changed in the gut of Amynthas corticis when the earthworm was incubated with pathogenic Escherichia coli O157:H7. Our genome assembly provides abundant and valuable resources for the earthworm research community, serving as a first step toward uncovering the mysteries of this species, and may provide molecular level indicators of its powerful defensive functions, adaptation to complex environments and invasion ability.
Topics: Animals; Escherichia coli; Evolution, Molecular; Gene Expression Regulation; Genome; Host-Pathogen Interactions; Oligochaeta; Phylogeny; Proteomics; Transcriptome
PubMed: 33514865
DOI: 10.1038/s42003-021-01659-4