Post-diapause transcriptomic restarts: insight from a high-latitude copepod

Abstract Background Diapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth. Emergence from diapause reverses the state of arrested development and metabolic suppression returning the organism to an active state. The...

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Published in:BMC Genomics
Main Authors: Roncalli, Vittoria, Cieslak, Matthew C., Castelfranco, Ann M., Hopcroft, Russell R., Hartline, Daniel K., Lenz, Petra H.
Other Authors: National Science Foundation
Format: Article in Journal/Newspaper
Language:English
Published: Springer Science and Business Media LLC 2021
Subjects:
Online Access:http://dx.doi.org/10.1186/s12864-021-07557-7
https://link.springer.com/content/pdf/10.1186/s12864-021-07557-7.pdf
https://link.springer.com/article/10.1186/s12864-021-07557-7/fulltext.html
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spelling crspringernat:10.1186/s12864-021-07557-7 2023-05-15T15:16:58+02:00 Post-diapause transcriptomic restarts: insight from a high-latitude copepod Roncalli, Vittoria Cieslak, Matthew C. Castelfranco, Ann M. Hopcroft, Russell R. Hartline, Daniel K. Lenz, Petra H. National Science Foundation 2021 http://dx.doi.org/10.1186/s12864-021-07557-7 https://link.springer.com/content/pdf/10.1186/s12864-021-07557-7.pdf https://link.springer.com/article/10.1186/s12864-021-07557-7/fulltext.html en eng Springer Science and Business Media LLC https://creativecommons.org/licenses/by/4.0 https://creativecommons.org/licenses/by/4.0 CC-BY BMC Genomics volume 22, issue 1 ISSN 1471-2164 Genetics Biotechnology journal-article 2021 crspringernat https://doi.org/10.1186/s12864-021-07557-7 2022-01-04T07:32:25Z Abstract Background Diapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth. Emergence from diapause reverses the state of arrested development and metabolic suppression returning the organism to an active state. The physiological mechanisms that regulate the transition from diapause to post-diapause are still unknown. In this study, this transition has been characterized for the sub-arctic calanoid copepod Neocalanus flemingeri , a key crustacean zooplankter that supports the highly productive North Pacific fisheries. Transcriptional profiling of females, determined over a two-week time series starting with diapausing females collected from > 400 m depth, characterized the molecular mechanisms that regulate the post-diapause trajectory. Results A complex set of transitions in relative gene expression defined the transcriptomic changes from diapause to post-diapause. Despite low temperatures (5–6 °C), the switch from a “diapause” to a “post-diapause” transcriptional profile occurred within 12 h of the termination stimulus. Transcriptional changes signaling the end of diapause were activated within one-hour post collection and included the up-regulation of genes involved in the 20E cascade pathway, the TCA cycle and RNA metabolism in combination with the down-regulation of genes associated with chromatin silencing. By 12 h, females exhibited a post-diapause phenotype characterized by the up-regulation of genes involved in cell division, cell differentiation and multiple developmental processes. By seven days post collection, the reproductive program was fully activated as indicated by up-regulation of genes involved in oogenesis and energy metabolism, processes that were enriched among the differentially expressed genes. Conclusions The analysis revealed a finely structured, precisely orchestrated sequence of transcriptional changes that led to rapid changes in the activation of biological processes paving the way to the successful completion of the reproductive program. Our findings lead to new hypotheses related to potentially universal mechanisms that terminate diapause before an organism can resume its developmental program. Article in Journal/Newspaper Arctic Springer Nature (via Crossref) Arctic Pacific BMC Genomics 22 1
institution Open Polar
collection Springer Nature (via Crossref)
op_collection_id crspringernat
language English
topic Genetics
Biotechnology
spellingShingle Genetics
Biotechnology
Roncalli, Vittoria
Cieslak, Matthew C.
Castelfranco, Ann M.
Hopcroft, Russell R.
Hartline, Daniel K.
Lenz, Petra H.
Post-diapause transcriptomic restarts: insight from a high-latitude copepod
topic_facet Genetics
Biotechnology
description Abstract Background Diapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth. Emergence from diapause reverses the state of arrested development and metabolic suppression returning the organism to an active state. The physiological mechanisms that regulate the transition from diapause to post-diapause are still unknown. In this study, this transition has been characterized for the sub-arctic calanoid copepod Neocalanus flemingeri , a key crustacean zooplankter that supports the highly productive North Pacific fisheries. Transcriptional profiling of females, determined over a two-week time series starting with diapausing females collected from > 400 m depth, characterized the molecular mechanisms that regulate the post-diapause trajectory. Results A complex set of transitions in relative gene expression defined the transcriptomic changes from diapause to post-diapause. Despite low temperatures (5–6 °C), the switch from a “diapause” to a “post-diapause” transcriptional profile occurred within 12 h of the termination stimulus. Transcriptional changes signaling the end of diapause were activated within one-hour post collection and included the up-regulation of genes involved in the 20E cascade pathway, the TCA cycle and RNA metabolism in combination with the down-regulation of genes associated with chromatin silencing. By 12 h, females exhibited a post-diapause phenotype characterized by the up-regulation of genes involved in cell division, cell differentiation and multiple developmental processes. By seven days post collection, the reproductive program was fully activated as indicated by up-regulation of genes involved in oogenesis and energy metabolism, processes that were enriched among the differentially expressed genes. Conclusions The analysis revealed a finely structured, precisely orchestrated sequence of transcriptional changes that led to rapid changes in the activation of biological processes paving the way to the successful completion of the reproductive program. Our findings lead to new hypotheses related to potentially universal mechanisms that terminate diapause before an organism can resume its developmental program.
author2 National Science Foundation
format Article in Journal/Newspaper
author Roncalli, Vittoria
Cieslak, Matthew C.
Castelfranco, Ann M.
Hopcroft, Russell R.
Hartline, Daniel K.
Lenz, Petra H.
author_facet Roncalli, Vittoria
Cieslak, Matthew C.
Castelfranco, Ann M.
Hopcroft, Russell R.
Hartline, Daniel K.
Lenz, Petra H.
author_sort Roncalli, Vittoria
title Post-diapause transcriptomic restarts: insight from a high-latitude copepod
title_short Post-diapause transcriptomic restarts: insight from a high-latitude copepod
title_full Post-diapause transcriptomic restarts: insight from a high-latitude copepod
title_fullStr Post-diapause transcriptomic restarts: insight from a high-latitude copepod
title_full_unstemmed Post-diapause transcriptomic restarts: insight from a high-latitude copepod
title_sort post-diapause transcriptomic restarts: insight from a high-latitude copepod
publisher Springer Science and Business Media LLC
publishDate 2021
url http://dx.doi.org/10.1186/s12864-021-07557-7
https://link.springer.com/content/pdf/10.1186/s12864-021-07557-7.pdf
https://link.springer.com/article/10.1186/s12864-021-07557-7/fulltext.html
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Pacific
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op_source BMC Genomics
volume 22, issue 1
ISSN 1471-2164
op_rights https://creativecommons.org/licenses/by/4.0
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op_rightsnorm CC-BY
op_doi https://doi.org/10.1186/s12864-021-07557-7
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