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Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming

SIMPLE SUMMARY: The reproductive processes of fish are known to be sensitive to water temperatures. However, the mechanism by which altered water temperature by river damming affects fish reproduction remains unclear. This study investigated the effects of altered water temperature on the developmen...

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Autores principales: Li, Ting, Chen, Qiuwen, Zhang, Qi, Feng, Tao, Zhang, Jianyun, Lin, Yuqing, Yang, Peisi, He, Shufeng, Zhang, Hui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9775624/
https://www.ncbi.nlm.nih.gov/pubmed/36552338
http://dx.doi.org/10.3390/biology11121829
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author Li, Ting
Chen, Qiuwen
Zhang, Qi
Feng, Tao
Zhang, Jianyun
Lin, Yuqing
Yang, Peisi
He, Shufeng
Zhang, Hui
author_facet Li, Ting
Chen, Qiuwen
Zhang, Qi
Feng, Tao
Zhang, Jianyun
Lin, Yuqing
Yang, Peisi
He, Shufeng
Zhang, Hui
author_sort Li, Ting
collection PubMed
description SIMPLE SUMMARY: The reproductive processes of fish are known to be sensitive to water temperatures. However, the mechanism by which altered water temperature by river damming affects fish reproduction remains unclear. This study investigated the effects of altered water temperature on the development of fish gonads by differential expression of temperature-sensitive transcripts. Particularly, the regulatory mechanism of oocyte meiotic division and the accumulation of nutrient materials were explored. We found that elevated temperatures, from a low value to a physiological optimum temperature, was conducive to cell division and vitellogenin accumulation; while elevated temperatures, from physiological optimum temperature to a high temperature within a certain range, was favorable for cell division but not vitellogenin accumulation. Although a warm winter temperature favors early gonadal development, it can impair final spawning quantity and quality in spring or summer. These results provide robust evidence that under the impacts of reservoir operation, the altered water temperature regime affects the gonadal development in temperate fish. ABSTRACT: Field investigation indicated that the reduction in fish spawning was associated with the alteration in water temperatures, even a 2–3 °C monthly difference due to reservoir operations. However, the physiological mechanism that influences the development of fish ovary (DFO) remains unclear. Thus, experiments of Coreius guichenoti were conducted at three different temperatures, optimal temperature (~20 °C, N) for fish spawning, lower (~17 °C, L), and higher (~23 °C, H), to reveal the effects of altered water temperature on the DFO. Comparisons were made between the L and N (LvsN) conditions and H and N (HvsN) conditions. Transcriptomic analysis differentially expressed transcripts (DETs) related to heat stress were observed only in LvsN conditions, indicating that the DFO showed a stronger response to changes in LvsN than in HvsN conditions. Upregulation of DETs of vitellogenin receptors in N temperature showed that normal temperature was conducive to vitellogenin entry into the oocytes. Other temperature-sensitive DETs, including microtubule, kinesin, dynein, and actin, were closely associated with cell division and material transport. LvsN significantly impacted cell division and nutrient accumulation in the yolk, whereas HvsN only influenced cell division. Our results highlight the impact of altered water temperature on the DFO, thereby providing insights for future reservoir operations regarding river damming and climate change and establishing fish conservation measures.
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spelling pubmed-97756242022-12-23 Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming Li, Ting Chen, Qiuwen Zhang, Qi Feng, Tao Zhang, Jianyun Lin, Yuqing Yang, Peisi He, Shufeng Zhang, Hui Biology (Basel) Article SIMPLE SUMMARY: The reproductive processes of fish are known to be sensitive to water temperatures. However, the mechanism by which altered water temperature by river damming affects fish reproduction remains unclear. This study investigated the effects of altered water temperature on the development of fish gonads by differential expression of temperature-sensitive transcripts. Particularly, the regulatory mechanism of oocyte meiotic division and the accumulation of nutrient materials were explored. We found that elevated temperatures, from a low value to a physiological optimum temperature, was conducive to cell division and vitellogenin accumulation; while elevated temperatures, from physiological optimum temperature to a high temperature within a certain range, was favorable for cell division but not vitellogenin accumulation. Although a warm winter temperature favors early gonadal development, it can impair final spawning quantity and quality in spring or summer. These results provide robust evidence that under the impacts of reservoir operation, the altered water temperature regime affects the gonadal development in temperate fish. ABSTRACT: Field investigation indicated that the reduction in fish spawning was associated with the alteration in water temperatures, even a 2–3 °C monthly difference due to reservoir operations. However, the physiological mechanism that influences the development of fish ovary (DFO) remains unclear. Thus, experiments of Coreius guichenoti were conducted at three different temperatures, optimal temperature (~20 °C, N) for fish spawning, lower (~17 °C, L), and higher (~23 °C, H), to reveal the effects of altered water temperature on the DFO. Comparisons were made between the L and N (LvsN) conditions and H and N (HvsN) conditions. Transcriptomic analysis differentially expressed transcripts (DETs) related to heat stress were observed only in LvsN conditions, indicating that the DFO showed a stronger response to changes in LvsN than in HvsN conditions. Upregulation of DETs of vitellogenin receptors in N temperature showed that normal temperature was conducive to vitellogenin entry into the oocytes. Other temperature-sensitive DETs, including microtubule, kinesin, dynein, and actin, were closely associated with cell division and material transport. LvsN significantly impacted cell division and nutrient accumulation in the yolk, whereas HvsN only influenced cell division. Our results highlight the impact of altered water temperature on the DFO, thereby providing insights for future reservoir operations regarding river damming and climate change and establishing fish conservation measures. MDPI 2022-12-15 /pmc/articles/PMC9775624/ /pubmed/36552338 http://dx.doi.org/10.3390/biology11121829 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Li, Ting
Chen, Qiuwen
Zhang, Qi
Feng, Tao
Zhang, Jianyun
Lin, Yuqing
Yang, Peisi
He, Shufeng
Zhang, Hui
Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title_full Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title_fullStr Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title_full_unstemmed Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title_short Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
title_sort transcriptomic analysis on the effects of altered water temperature regime on the fish ovarian development of coreius guichenoti under the impact of river damming
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9775624/
https://www.ncbi.nlm.nih.gov/pubmed/36552338
http://dx.doi.org/10.3390/biology11121829
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