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Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily

BACKGROUND: The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. However, our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. Here we present a unique insight into t...

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Autores principales: Hyde, Cameron J., Fitzgibbon, Quinn P., Elizur, Abigail, Smith, Gregory G., Ventura, Tomer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6599367/
https://www.ncbi.nlm.nih.gov/pubmed/31253104
http://dx.doi.org/10.1186/s12864-019-5925-5
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author Hyde, Cameron J.
Fitzgibbon, Quinn P.
Elizur, Abigail
Smith, Gregory G.
Ventura, Tomer
author_facet Hyde, Cameron J.
Fitzgibbon, Quinn P.
Elizur, Abigail
Smith, Gregory G.
Ventura, Tomer
author_sort Hyde, Cameron J.
collection PubMed
description BACKGROUND: The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. However, our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. Here we present a unique insight into the molecular pathways coordinating crustacean metamorphosis, by reconciling nuclear receptor (NR) gene activity from a 12-stage, 3-replicate transcriptome in the ornate spiny lobster (Panulirus ornatus) during larval development. RESULTS: We annotated 18 distinct nuclear receptor genes, including three novel NRs which are upregulated prior to metamorphosis and have hence been named the “molt-associated receptors” (MARs). We also demonstrate the ecdysone-responsive expression of several known molt-related NRs including ecdysone receptor, fushi-tarazu-F1 and E75. Phylogenetic analysis of the curated NR family confirmed gene annotations and suggested that the MARs are a recent addition to the crustacean superfamily, occurring across the Malacostraca from the Stomatopoda to the Decapoda. The ligand-binding domain of these receptors appears to be less conserved than that of typical group-1 NRs. Expression data from two other crustacean species was utilized to examine MAR expression. The Y-organ of the tropical land crab showed a decline in expression of all MARs from intermolt to post-molt. Tissue distributions showed gonad-enriched expression in the Eastern rock lobster and antennal gland-enriched expression in the tropical land crab, although expression was evident across most tissues. CONCLUSION: By mining transcriptome data, we have curated an extensive list of NR genes expressed during the metamorphic molts of P. ornatus, including three novel crustacean NRs which appear to play a role in the molting process. Divergence of the E-region of these new receptors indicates that they may have adopted a function that is unconventional for NRs. Based on expression patterns, we can confirm that a number of NRs play a role in the ecdysone cassette which regulates molting in crustaceans. This study describes in detail the molecular events surrounding crustacean molting and metamorphosis by taking advantage of the distinctive life history unique to achelatan crustaceans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5925-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-65993672019-07-11 Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily Hyde, Cameron J. Fitzgibbon, Quinn P. Elizur, Abigail Smith, Gregory G. Ventura, Tomer BMC Genomics Research Article BACKGROUND: The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. However, our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. Here we present a unique insight into the molecular pathways coordinating crustacean metamorphosis, by reconciling nuclear receptor (NR) gene activity from a 12-stage, 3-replicate transcriptome in the ornate spiny lobster (Panulirus ornatus) during larval development. RESULTS: We annotated 18 distinct nuclear receptor genes, including three novel NRs which are upregulated prior to metamorphosis and have hence been named the “molt-associated receptors” (MARs). We also demonstrate the ecdysone-responsive expression of several known molt-related NRs including ecdysone receptor, fushi-tarazu-F1 and E75. Phylogenetic analysis of the curated NR family confirmed gene annotations and suggested that the MARs are a recent addition to the crustacean superfamily, occurring across the Malacostraca from the Stomatopoda to the Decapoda. The ligand-binding domain of these receptors appears to be less conserved than that of typical group-1 NRs. Expression data from two other crustacean species was utilized to examine MAR expression. The Y-organ of the tropical land crab showed a decline in expression of all MARs from intermolt to post-molt. Tissue distributions showed gonad-enriched expression in the Eastern rock lobster and antennal gland-enriched expression in the tropical land crab, although expression was evident across most tissues. CONCLUSION: By mining transcriptome data, we have curated an extensive list of NR genes expressed during the metamorphic molts of P. ornatus, including three novel crustacean NRs which appear to play a role in the molting process. Divergence of the E-region of these new receptors indicates that they may have adopted a function that is unconventional for NRs. Based on expression patterns, we can confirm that a number of NRs play a role in the ecdysone cassette which regulates molting in crustaceans. This study describes in detail the molecular events surrounding crustacean molting and metamorphosis by taking advantage of the distinctive life history unique to achelatan crustaceans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5925-5) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-28 /pmc/articles/PMC6599367/ /pubmed/31253104 http://dx.doi.org/10.1186/s12864-019-5925-5 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Hyde, Cameron J.
Fitzgibbon, Quinn P.
Elizur, Abigail
Smith, Gregory G.
Ventura, Tomer
Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title_full Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title_fullStr Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title_full_unstemmed Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title_short Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
title_sort transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6599367/
https://www.ncbi.nlm.nih.gov/pubmed/31253104
http://dx.doi.org/10.1186/s12864-019-5925-5
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