Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus

Introduction Calanus finmarchicus, a highly abundant copepod that is an important primary consumer in North Atlantic ecosystems, has a flexible life history in which copepods in the last juvenile developmental stage (fifth copepodid, C5) may either delay maturation and enter diapause or molt directl...

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Published in:Frontiers in Zoology
Main Authors: Tarrant, Ann, Baumgartner, Mark, Hansen, Bjørn Henrik, Altin, Dag, Nordtug, Trond, Olsen, Anders Johny
Format: Article in Journal/Newspaper
Language:English
Published: 2014
Subjects:
Online Access:http://hdl.handle.net/11250/2585774
https://doi.org/10.1186/s12983-014-0091-8
id ftsintef:oai:sintef.brage.unit.no:11250/2585774
record_format openpolar
institution Open Polar
collection SINTEF Open (Brage)
op_collection_id ftsintef
language English
topic Arthropod
Crustacean
Gene expression
Molt cycle
Transcriptomics
spellingShingle Arthropod
Crustacean
Gene expression
Molt cycle
Transcriptomics
Tarrant, Ann
Baumgartner, Mark
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders Johny
Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
topic_facet Arthropod
Crustacean
Gene expression
Molt cycle
Transcriptomics
description Introduction Calanus finmarchicus, a highly abundant copepod that is an important primary consumer in North Atlantic ecosystems, has a flexible life history in which copepods in the last juvenile developmental stage (fifth copepodid, C5) may either delay maturation and enter diapause or molt directly into adults. The factors that regulate this developmental plasticity are poorly understood, and few tools have been developed to assess the physiological condition of individual copepods. Results We sampled a cultured population of C. finmarchicus copepods daily throughout the C5 stage and assessed molt stage progression, gonad development and lipid storage. We used high-throughput sequencing to identify genes that were differentially expressed during progression through the molt stage and then used qPCR to profile daily expression of individual genes. Based on expression profiles of twelve genes, samples were statistically clustered into three groups: (1) an early period occurring prior to separation of the cuticle from the epidermis (apolysis) when expression of genes associated with lipid synthesis and transport (FABP and ELOV) and two nuclear receptors (ERR and HR78) was highest, (2) a middle period of rapid change in both gene expression and physiological condition, including local minima and maxima in several nuclear receptors (FTZ-F1, HR38b, and EcR), and (3) a late period when gonads were differentiated and expression of genes associated with molting (Torso-like, HR38a) peaked. The ratio of Torso-like to HR38b strongly differentiated the early and late groups. Conclusions This study provides the first dynamic profiles of gene expression anchored with morphological markers of lipid accumulation, development and gonad maturation throughout a copepod molt cycle. Transcriptomic profiling revealed significant changes over the molt cycle in genes with presumed roles in lipid synthesis, molt regulation and gonad development, suggestive of a coupling of these processes in Calanus finmarchicus. Finally, we identified gene expression profiles that strongly differentiate between early and late development within the C5 copepodid stage. We anticipate that these findings and continued development of robust gene expression biomarkers that distinguish between diapause preparation and continuous development will ultimately enable novel studies of the intrinsic and extrinsic factors that govern diapause initiation in Calanus finmarchicus. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus publishedVersion
format Article in Journal/Newspaper
author Tarrant, Ann
Baumgartner, Mark
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders Johny
author_facet Tarrant, Ann
Baumgartner, Mark
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders Johny
author_sort Tarrant, Ann
title Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title_short Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title_full Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title_fullStr Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title_full_unstemmed Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title_sort transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod calanus finmarchicus
publishDate 2014
url http://hdl.handle.net/11250/2585774
https://doi.org/10.1186/s12983-014-0091-8
genre Calanus finmarchicus
North Atlantic
Copepods
genre_facet Calanus finmarchicus
North Atlantic
Copepods
op_source 15
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Frontiers in Zoology
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op_relation Frontiers in Zoology. 2014, 11 (1), .
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© 2014 Tarrant et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
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spelling ftsintef:oai:sintef.brage.unit.no:11250/2585774 2023-05-15T15:47:52+02:00 Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus Tarrant, Ann Baumgartner, Mark Hansen, Bjørn Henrik Altin, Dag Nordtug, Trond Olsen, Anders Johny 2014-12-16 application/pdf http://hdl.handle.net/11250/2585774 https://doi.org/10.1186/s12983-014-0091-8 eng eng Frontiers in Zoology. 2014, 11 (1), . urn:issn:1742-9994 http://hdl.handle.net/11250/2585774 https://doi.org/10.1186/s12983-014-0091-8 cristin:1193421 Navngivelse 4.0 Internasjonal http://creativecommons.org/licenses/by/4.0/deed.no © 2014 Tarrant et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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. CC-BY CC0 PDM 15 11 Frontiers in Zoology 1 Arthropod Crustacean Gene expression Molt cycle Transcriptomics Journal article Peer reviewed 2014 ftsintef https://doi.org/10.1186/s12983-014-0091-8 2021-08-04T12:00:17Z Introduction Calanus finmarchicus, a highly abundant copepod that is an important primary consumer in North Atlantic ecosystems, has a flexible life history in which copepods in the last juvenile developmental stage (fifth copepodid, C5) may either delay maturation and enter diapause or molt directly into adults. The factors that regulate this developmental plasticity are poorly understood, and few tools have been developed to assess the physiological condition of individual copepods. Results We sampled a cultured population of C. finmarchicus copepods daily throughout the C5 stage and assessed molt stage progression, gonad development and lipid storage. We used high-throughput sequencing to identify genes that were differentially expressed during progression through the molt stage and then used qPCR to profile daily expression of individual genes. Based on expression profiles of twelve genes, samples were statistically clustered into three groups: (1) an early period occurring prior to separation of the cuticle from the epidermis (apolysis) when expression of genes associated with lipid synthesis and transport (FABP and ELOV) and two nuclear receptors (ERR and HR78) was highest, (2) a middle period of rapid change in both gene expression and physiological condition, including local minima and maxima in several nuclear receptors (FTZ-F1, HR38b, and EcR), and (3) a late period when gonads were differentiated and expression of genes associated with molting (Torso-like, HR38a) peaked. The ratio of Torso-like to HR38b strongly differentiated the early and late groups. Conclusions This study provides the first dynamic profiles of gene expression anchored with morphological markers of lipid accumulation, development and gonad maturation throughout a copepod molt cycle. Transcriptomic profiling revealed significant changes over the molt cycle in genes with presumed roles in lipid synthesis, molt regulation and gonad development, suggestive of a coupling of these processes in Calanus finmarchicus. Finally, we identified gene expression profiles that strongly differentiate between early and late development within the C5 copepodid stage. We anticipate that these findings and continued development of robust gene expression biomarkers that distinguish between diapause preparation and continuous development will ultimately enable novel studies of the intrinsic and extrinsic factors that govern diapause initiation in Calanus finmarchicus. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus publishedVersion Article in Journal/Newspaper Calanus finmarchicus North Atlantic Copepods SINTEF Open (Brage) Frontiers in Zoology 11 1