Cargando…

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 direct...

Descripción completa

Detalles Bibliográficos
Autores principales: Tarrant, Ann M, Baumgartner, Mark F, Hansen, Bjørn Henrik, Altin, Dag, Nordtug, Trond, Olsen, Anders J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4285635/
https://www.ncbi.nlm.nih.gov/pubmed/25568661
http://dx.doi.org/10.1186/s12983-014-0091-8
_version_ 1782351579288961024
author Tarrant, Ann M
Baumgartner, Mark F
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders J
author_facet Tarrant, Ann M
Baumgartner, Mark F
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders J
author_sort Tarrant, Ann M
collection PubMed
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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-014-0091-8) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4285635
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-42856352015-01-08 Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus Tarrant, Ann M Baumgartner, Mark F Hansen, Bjørn Henrik Altin, Dag Nordtug, Trond Olsen, Anders J Front Zool Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-014-0091-8) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-16 /pmc/articles/PMC4285635/ /pubmed/25568661 http://dx.doi.org/10.1186/s12983-014-0091-8 Text en © Tarrant et al.; licensee BioMed Central. 2014 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.
spellingShingle Research
Tarrant, Ann M
Baumgartner, Mark F
Hansen, Bjørn Henrik
Altin, Dag
Nordtug, Trond
Olsen, Anders J
Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus
title 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_short 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
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4285635/
https://www.ncbi.nlm.nih.gov/pubmed/25568661
http://dx.doi.org/10.1186/s12983-014-0091-8
work_keys_str_mv AT tarrantannm transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus
AT baumgartnermarkf transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus
AT hansenbjørnhenrik transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus
AT altindag transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus
AT nordtugtrond transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus
AT olsenandersj transcriptionalprofilingofreproductivedevelopmentlipidstorageandmoltingthroughoutthelastjuvenilestageofthemarinecopepodcalanusfinmarchicus