Transcriptome analysis elucidates key developmental components of bryozoan lophophore development

The most recent phylogenomic study suggested that Bryozoa (Ectoprocta), Brachiopoda and Phoronida are monophyletic, implying that the lophophore of bryozoans, phoronids and brachiopods is a synapomorphy. Understanding the molecular mechanisms of the lophophore development of the Lophophorata clade can therefore provide us a new insight into the formation of the diverse morphological traits in metazoans. In the present study, we profiled the transcriptome of the Bryozoan (Ectoproct) Bugula neritina during the swimming larval stage (SW) and the early (4 h) and late (24 h) metamorphic stages using the Illumina HiSeq2000 platform. Various genes that function in development, the immune response and neurogenesis showed differential expression levels during metamorphosis. In situ hybridization of 23 genes that participate in the Wnt, BMP, Notch and Hedgehog signaling pathways revealed their regulatory roles in the development of the lophophore and the ancestrula digestive tract. Our findings support the hypothesis that developmental precursors of the lophophore and the ancestrula digestive tract are pre-patterned by the differential expression of key developmental genes according to their fate. This study provides a foundation to better understand the developmental divergence and/or convergence among developmental precursors of the lophophore of bryozoans, branchiopods and phoronids.

• Publication year

  2014

• Venue

  Scientific Reports

• Publication date

  2014-10-10

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/srep06534PMID 25300304PMCID 4192642
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration

  2013cited by this paper
• CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model

  2013cited by this paper
• New phylogenomic data support the monophyly of Lophophorata and an Ectoproct-Phoronid clade and indicate that Polyzoa and Kryptrochozoa are caused by systematic bias

  2013cited by this paper
• Musical Training Induces Functional Plasticity in Perceptual and Motor Networks: Insights from Resting-State fMRI

  2012cited by this paper
• GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data

  2012cited by this paper
• CD-HIT: accelerated for clustering the next-generation sequencing data

  2012cited by this paper
• Direct Comparisons of Illumina vs. Roche 454 Sequencing Technologies on the Same Microbial Community DNA Sample

  2012cited by this paper
• Development of the nervous system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals both deuterostome- and trochozoan-like features

  2012cited by this paper
• Developmental plasticity and the evolution of parasitism in an unusual nematode, Parastrongyloides trichosuri

  2012cited by this paper
• The Notch signalling system: recent insights into the complexity of a conserved pathway

  2012cited by this paper
• Development of the larval anterior neurogenic domains of Terebratalia transversa (Brachiopoda) provides insights into the diversification of larval apical organs and the spiralian nervous system

  2012cited by this paper
• Involvement of Wnt Signaling Pathways in the Metamorphosis of the Bryozoan Bugula neritina

  2012influential reference
• Fast gapped-read alignment with Bowtie 2

  2012cited by this paper
• Memory, Visual Discrimination Performance, and the Human Hippocampus

  2011cited by this paper
• NONCODE v3.0: integrative annotation of long noncoding RNAs

  2011cited by this paper
• Gene expression in bryozoan larvae suggest a fundamental importance of pre-patterned blastemic cells in the bryozoan life-cycle

  2011cited by this paper
• De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics.

  2011cited by this paper
• Quantitative proteomics identify molecular targets that are crucial in larval settlement and metamorphosis of Bugula neritina.

  2011cited by this paper
• Evaluating neurophylogenetic patterns in the larval nervous systems of brachiopods and their evolutionary significance to other bilaterian phyla

  2011cited by this paper
• Structure and occurrence of cyphonautes larvae (bryozoa, ectoprocta)

  2010cited by this paper
• De novo assembly and analysis of RNA-seq data

  2010cited by this paper
• Reactome: a database of reactions, pathways and biological processes

  2010cited by this paper
• Rapid transcriptome and proteome profiling of a non‐model marine invertebrate, Bugula neritina

  2010cited by this paper
• Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida).

  2010cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009cited by this paper
• ABySS: a parallel assembler for short read sequence data.

  2009cited by this paper
• Broad phylogenomic sampling improves resolution of the animal tree of life

  2008cited by this paper
• Hedgehog signaling pathway function conserved in Tribolium segmentation

  2008cited by this paper
• Phylogenetic position of Nemertea derived from phylogenomic data.

  2008cited by this paper
• Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata)

  2008cited by this paper
• Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept

  2008cited by this paper
• InterPro and InterProScan

  2007cited by this paper
• Integration of biological networks and gene expression data using Cytoscape

  2007cited by this paper
• InterPro and InterProScan: tools for protein sequence classification and comparison.

  2007cited by this paper
• High-resolution in situ hybridization to whole-mount zebrafish embryos

  2007cited by this paper
• Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning.

  2006cited by this paper
• Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis

  2005cited by this paper
• FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left–right determination

  2005cited by this paper
• Immunocytochemistry and metamorphic fate of the larval nervous system of Triphyllozoon mucronatum (Ectoprocta: Gymnolaemata: Cheilostomata)

  2005cited by this paper
• Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs.

  2004cited by this paper
• An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation

  2003cited by this paper
• Invertebrates

  2003cited by this paper
• The Phylogenetic Position of Entoprocta, Ectoprocta, Phoronida, and Brachiopoda1

  2002cited by this paper
• A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response.

  2002cited by this paper
• Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida)

  2002cited by this paper
• The human genome browser at UCSC.

  2002cited by this paper
• Kremen proteins interact with Dickkopf1 to regulate anteroposterior CNS patterning

  2002cited by this paper
• BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors.

  2002cited by this paper
• Divergence and convergence of TGF‐β/BMP signaling

  2001cited by this paper
• BIOINFORMATICS APPLICATIONS NOTE

  2001cited by this paper
• Heads or tails: Wnts and anterior-posterior patterning.

  2001cited by this paper
• EMBOSS: the European Molecular Biology Open Software Suite.

  2000cited by this paper
• Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity.

  2000cited by this paper
• Gene Ontology: tool for the unification of biology

  2000cited by this paper
• The development of the musculature in the limpet Patella with implications on its role in the process of ontogenetic torsion

  1999cited by this paper
• IL-17 Stimulates the Production and Expression of Proinflammatory Cytokines, IL-β and TNF-α, by Human Macrophages

  1998cited by this paper
• IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages.

  1998cited by this paper
• Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4.

  1996cited by this paper
• Contribution of phosphocreatine and aerobic metabolism to energy supply during repeated sprint exercise.

  1996cited by this paper
• Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn-2.

  1995cited by this paper
• Evidence from 18S ribosomal DNA that the lophophorates are protostome animals

  1995cited by this paper
• Chitosan-mediated stimulation of macrophage function.

  1994cited by this paper
• Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone, Haliotis rufescens.

  1992cited by this paper
• Basic local alignment search tool.

  1990cited by this paper
• The gastropod nervous system in metamorphosis.

  1990cited by this paper
• Involvement of the Xenopus homeobox gene Xhox3 in pattern formation along the anterior-posterior axis.

  1989cited by this paper
• Attachment and metamorphosis of the cheilo‐ctenostome bryozoan bugula neritina (linné)

  1971cited by this paper
• Abyss: a Parallel Assembler for Short Read Sequence Data Material Supplemental Open Access

  year unknowncited by this paper

• Transcriptomic Landscape of Polypide Development in the Freshwater Bryozoan Cristatella mucedo: From Budding to Degeneration.

  2025cites this paper
• Unravelling the pharmacological applications and taxonomical challenges in Canscora species using DNA barcodes (taxon-specific DNA and high-throughput DNA barcodes): a systematic review

  2025cites this paper
• The genome sequence of the ruby bryozoan, Bugula neritina (Linnaeus, 1758)

  2024cites this paper
• Emerging trends in the study of spiralian larvae

  2023cites this paper
• Stage-Specific Transcriptomes of the Mussel Mytilus coruscus Reveals the Developmental Program for the Planktonic to Benthic Transition

  2023cites this paper
• Behavioral and transcriptomic changes in butenolide treated larvae of the cosmopolitan fouling bryozoan Bugulina (Bugula) neritina

  2022cites this paper
• Transcriptome analysis elucidates key changes of pleon in the process of carcinization

  2021cites this paper
• Transcriptome analysis provides insights into a molecular mechanism of histamine response in the cyprid larvae of Amphibalanus amphitrite

  2021cites this paper
• The evolution of the metazoan Toll receptor family and its expression during protostome development

  2021cites this paper
• Differential Gene Expression Between Polymorphic Zooids of the Marine Bryozoan Bugulina stolonifera

  2020influential citation
• Transcriptomic analysis of the mode of action of the candidate anti-fouling compound di(1H-indol-3-yl)methane (DIM) on a marine biofouling species, the bryozoan Bugula neritina.

  2020cites this paper
• First transcriptome analysis of bryozoan Fredericella sultana, the primary host of myxozoan parasite Tetracapsuloides bryosalmonae

  2020cites this paper
• Draft genome of Bugula neritina, a colonial animal packing powerful symbionts and potential medicines

  2020cites this paper
• Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour

  2019cites this paper
• Diversity and Dynamics of “Candidatus Endobugula” and Other Symbiotic Bacteria in Chinese Populations of the Bryozoan, Bugula neritina

  2018cites this paper
• The regulatory role of arginine kinase during larval settlement of the bryozoan Bugula neritina

  2018cites this paper
• The regulatory role of arginine kinase during larval settlement of the bryozoan Bugula neritina

  2018cites this paper
• Exploring the regulatory role of nitric oxide (NO) and the NO-p38MAPK/cGMP pathway in larval settlement of the bryozoan Bugula neritina

  2018cites this paper
• Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

  2017cites this paper
• In Silico Prediction of Neuropeptides/Peptide Hormone Transcripts in the Cheilostome Bryozoan Bugula neritina

  2016cites this paper
• The Importance of Next-generation Sequencing for Marine Larvae Research: Insight into Larvae Settlement and Anti-fouling

  2016cites this paper
• Transcriptomic Analysis of the Endangered Neritid Species Clithon retropictus: De Novo Assembly, Functional Annotation, and Marker Discovery

  2016cites this paper
• Investigation of larval sensory systems in the marine bryozoan, Bugula neritina

  2015cites this paper