The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra

Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Mishima, Shizuoka 411-8540 Japan.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 10/2007; 104(37):14735-40. DOI: 10.1073/pnas.0703331104
Source: PubMed


Cell lineages of cnidarians including Hydra represent the fundamental cell types of metazoans and provides us a unique opportunity to study the evolutionary diversification of cell type in the animal kingdom. Hydra contains epithelial cells as well as a multipotent interstitial cell (I-cell) that gives rise to nematocytes, nerve cells, gland cells, and germ-line cells. We used cDNA microarrays to identify cell type-specific genes by comparing gene expression in normal Hydra with animals lacking the I-cell lineage, so-called epithelial Hydra. We then performed in situ hybridization to localize expression to specific cell types. Eighty-six genes were shown to be expressed in specific cell types of the I-cell lineage. An additional 29 genes were expressed in epithelial cells and were down-regulated in epithelial animals lacking I-cells. Based on the above information, we constructed a database (, which describes the expression patterns of cell type-specific genes in Hydra. Most genes expressed specifically in either I-cells or epithelial cells have homologues in higher metazoans. By comparison, most nematocyte-specific genes and approximately half of the gland cell- and nerve cell-specific genes are unique to the cnidarian lineage. Because nematocytes, gland cells, and nerve cells appeared along with the emergence of cnidarians, this suggests that lineage-specific genes arose in cnidarians in conjunction with the evolution of new cell types required by the cnidarians.

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    • "We localized the expression of miR-2022 and its target Nematogalectinrelated 2 (NR2), miR-2026 and its target HoxD, miR-2030 and its target NVE19315, and miR-2025 and its targets Six3/6 and NVE8472 (Fig. 5A). NR2 encodes a protein found in the tubule of the nematocyst, the stinging organelle typifying Cnidaria (Hwang et al. 2007). Both NR2 and miR-2022 colocalized to nematocytes, the cells containing nematocysts (Fig. 5A). "
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    ABSTRACT: In bilaterians, which comprise most of extant animals, microRNAs (miRNAs) regulate the majority of messenger RNAs (mRNAs) via base-pairing of a short sequence (the miRNA "seed") to the target, subsequently promoting translational inhibition and transcript instability. In plants, many miRNAs guide endonucleolytic cleavage of highly complementary targets. Because little is known about miRNA function in nonbilaterian animals, we investigated the repertoire and biological activity of miRNAs in the sea anemone Nematostella vectensis, a representative of Cnidaria, the sister phylum of Bilateria. Our work uncovers scores of novel miRNAs in Nematostella, increasing the total miRNA gene count to 87. Yet only a handful are conserved in corals and hydras, suggesting that microRNA gene turnover in Cnidaria greatly exceeds that of other metazoan groups. We further show that Nematostella miRNAs frequently direct the cleavage of their mRNA targets via nearly perfect complementarity. This mode of action resembles that of small interfering RNAs (siRNAs) and plant miRNAs. It appears to be common in Cnidaria, as several of the miRNA target sites are conserved among distantly related anemone species, and we also detected miRNA-directed cleavage in Hydra. Unlike in bilaterians, Nematostella miRNAs are commonly coexpressed with their target transcripts. In light of these findings, we propose that post-transcriptional regulation by miRNAs functions differently in Cnidaria and Bilateria. The similar, siRNA-like mode of action of miRNAs in Cnidaria and plants suggests that this may be an ancestral state.
    Genome Research 03/2014; 24(4). DOI:10.1101/gr.162503.113 · 14.63 Impact Factor
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    • "Among cnidarians, genomic data are currently available from three species, Hydra magnipapillata[3], Nematostella vectensis (sea anemone) [4] and Acropora digitifera (coral) [5]. Transcriptomic data are available from the colonial hydroid Hydractinia equinata[6], from the jellyfish Clytia haemispherica[7], from the coral Acropora millepora[8,9] and from two distinct Hydra strains that belong to the heterogeneous vulgaris group [10,11]. In addition, two sets of putative transcripts, called here pred-CA and pred-RP, have been predicted from the Hydra magnipapillata genome [3]. "
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    ABSTRACT: Background: Evolutionary studies benefit from deep sequencing technologies that generate genomic and transcriptomic sequences from a variety of organisms. Genome sequencing and RNAseq have complementary strengths. In this study, we present the assembly of the most complete Hydra transcriptome to date along with a comparative analysis of the specific features of RNAseq and genome-predicted transcriptomes currently available in the freshwater hydrozoan Hydra vulgaris. Results: To produce an accurate and extensive Hydra transcriptome, we combined Illumina and 454 Titanium reads, giving the primacy to Illumina over 454 reads to correct homopolymer errors. This strategy yielded an RNAseq transcriptome that contains 48'909 unique sequences including splice variants, representing approximately 24'450 distinct genes. Comparative analysis to the available genome-predicted transcriptomes identified 10'597 novel Hydra transcripts that encode 529 evolutionarily-conserved proteins. The annotation of 170 human orthologs points to critical functions in protein biosynthesis, FGF and TOR signaling, vesicle transport, immunity, cell cycle regulation, cell death, mitochondrial metabolism, transcription and chromatin regulation. However, a majority of these novel transcripts encodes short ORFs, at least 767 of them corresponding to pseudogenes. This RNAseq transcriptome also lacks 11'270 predicted transcripts that correspond either to silent genes or to genes expressed below the detection level of this study. Conclusions: We established a simple and powerful strategy to combine Illumina and 454 reads and we produced, with genome assistance, an extensive and accurate Hydra transcriptome. The comparative analysis of the RNAseq transcriptome with genome-predicted transcriptomes lead to the identification of large populations of novel as well as missing transcripts that might reflect Hydra-specific evolutionary events.
    BMC Genomics 03/2013; 14(1):204. DOI:10.1186/1471-2164-14-204 · 3.99 Impact Factor
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    • "This is a strong enrichment compared to results from recent re-annotation of the Nematostella transcriptome that found 16 % of the protein models to lack metazoan homologues and 5 % to lack both homologues and conserved domains (Fredman D. and Technau U. unpublished results). This is consistent with genetic studies in Hydra, indicating that a substantial fraction of the genes exclusively expressed in nematocytes are TRGs (Hwang et al. 2007; Milde et al. 2009). As the nematocyst is a unique cnidarian structure conserved for more than 600 million years it is plausible that many of its component proteins including toxins will be encoded by TRGs. "
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    ABSTRACT: The nematocyst is one of the most complex intracellular structures found in nature and is the defining feature of the phylum Cnidaria (sea anemones, corals, jellyfish, and hydroids). This miniature stinging organelle contains and delivers venom into prey and foe yet little is known about its toxic components. In the present study, we identified by tandem mass spectrometry 20 proteins released upon discharge from the nematocyst of the model sea anemone Nematostella vectensis. The availability of genomic and transcriptomic data for this species enabled accurate identification and phylogenetic study of these components. Fourteen of these proteins could not be identified in other animals suggesting that they might be the products of taxonomically restricted genes, a finding which fits well their origin from a taxon-specific organelle. Further, we studied by in situ hybridization the localization of two of the transcripts encoding the putative nematocyst venom proteins: a metallopeptidase related to the Tolloid family and a cysteine-rich protein. Both transcripts were detected in nematocytes, which are the cells containing nematocysts, and the metallopeptidase was found also in pharyngeal gland cells. Our findings reveal for the first time the possible venom components of a sea anemone nematocyst and suggest their evolutionary origins. Electronic supplementary material The online version of this article (doi:10.1007/s10126-012-9491-y) contains supplementary material, which is available to authorized users.
    Marine Biotechnology 11/2012; 15(3). DOI:10.1007/s10126-012-9491-y · 3.27 Impact Factor
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