Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)

Smolting is an important development stage of salmonid, and an energy trade-off occurs between osmotic regulation and growth during smolting in rainbow trout (<i>Oncorhynchus mykiss</i>). Growth hormone releasing hormone, somatostatin, growth hormone and insulin-like growth factor (GHRH-...

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Main Authors: Kaiwen Xiang, Qian Yang, Mengqun Liu, Xiaodong Yang, Jifang Li, Zhishuai Hou, Haishen Wen
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/15/8691
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author Kaiwen Xiang
Qian Yang
Mengqun Liu
Xiaodong Yang
Jifang Li
Zhishuai Hou
Haishen Wen
author_facet Kaiwen Xiang
Qian Yang
Mengqun Liu
Xiaodong Yang
Jifang Li
Zhishuai Hou
Haishen Wen
author_sort Kaiwen Xiang
collection DOAJ
description Smolting is an important development stage of salmonid, and an energy trade-off occurs between osmotic regulation and growth during smolting in rainbow trout (<i>Oncorhynchus mykiss</i>). Growth hormone releasing hormone, somatostatin, growth hormone and insulin-like growth factor (GHRH-SST-GH-IGF) axis exhibit pleiotropic effects in regulating growth and osmotic adaptation. Due to salmonid specific genome duplication, increased paralogs are identified in the <i>ghrh</i>-<i>sst-gh</i>-<i>igf</i> axis, however, their physiology in modulating osmoregulation has yet to be investigated. In this study, seven <i>sst</i> genes (<i>sst1a</i>, <i>sst1b</i>, <i>sst2</i>, <i>sst3a</i>, <i>sst3b</i>, <i>sst5</i>, <i>sst6</i>) were identified in trout. We further investigated the <i>ghrh</i>-<i>sst-gh</i>-<i>igf</i> axis of diploid and triploid trout in response to seawater challenge. Kidney <i>sst</i> (<i>sst1b</i>, <i>sst2</i>, <i>sst5</i>) and <i>sstr</i> (<i>sstr1b1</i>, <i>sstr5a</i>, <i>sstr5b</i>) expressions were changed (more than 2-fold increase (except for <i>sstr5a</i> with 1.99-fold increase) or less than 0.5-fold decrease) due to osmoregulation, suggesting a pleiotropic physiology of SSTs in modulating growth and smoltification. Triploid trout showed significantly down-regulated brain <i>sstr1b1</i> and <i>igfbp2a1</i> (<i>p</i> < 0.05), while diploid trout showed up-regulated brain <i>igfbp1a1</i> (~2.61-fold, <i>p</i> = 0.057) and <i>igfbp2a</i> subtypes (~1.38-fold, <i>p</i> < 0.05), suggesting triploid trout exhibited a better acclimation to the seawater environment. The triploid trout showed up-regulated kidney <i>igfbp5a</i> subtypes (~6.62 and 7.25-fold, <i>p</i> = 0.099 and 0.078) and significantly down-regulated <i>igfbp5b2</i> (~0.37-fold, <i>p</i> < 0.05), showing a conserved physiology of teleost IGFBP5a in regulating osmoregulation. The IGFBP6 subtypes are involved in energy and nutritional regulation. Distinctive <i>igfbp6</i> subtypes patterns (<i>p</i> < 0.05) potentially indicated trout triggered energy redistribution in brain and kidney during osmoregulatory regulation. In conclusion, we showed that the GHRH-SST-GH-IGF axis exhibited pleiotropic effects in regulating growth and osmoregulatory regulation during trout smolting, which might provide new insights into seawater aquaculture of salmonid species.
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spelling doaj.art-aebedea900b84b52a7c3e241faa0b66f2023-12-03T12:41:28ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-08-012315869110.3390/ijms23158691Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)Kaiwen Xiang0Qian Yang1Mengqun Liu2Xiaodong Yang3Jifang Li4Zhishuai Hou5Haishen Wen6Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, ChinaSmolting is an important development stage of salmonid, and an energy trade-off occurs between osmotic regulation and growth during smolting in rainbow trout (<i>Oncorhynchus mykiss</i>). Growth hormone releasing hormone, somatostatin, growth hormone and insulin-like growth factor (GHRH-SST-GH-IGF) axis exhibit pleiotropic effects in regulating growth and osmotic adaptation. Due to salmonid specific genome duplication, increased paralogs are identified in the <i>ghrh</i>-<i>sst-gh</i>-<i>igf</i> axis, however, their physiology in modulating osmoregulation has yet to be investigated. In this study, seven <i>sst</i> genes (<i>sst1a</i>, <i>sst1b</i>, <i>sst2</i>, <i>sst3a</i>, <i>sst3b</i>, <i>sst5</i>, <i>sst6</i>) were identified in trout. We further investigated the <i>ghrh</i>-<i>sst-gh</i>-<i>igf</i> axis of diploid and triploid trout in response to seawater challenge. Kidney <i>sst</i> (<i>sst1b</i>, <i>sst2</i>, <i>sst5</i>) and <i>sstr</i> (<i>sstr1b1</i>, <i>sstr5a</i>, <i>sstr5b</i>) expressions were changed (more than 2-fold increase (except for <i>sstr5a</i> with 1.99-fold increase) or less than 0.5-fold decrease) due to osmoregulation, suggesting a pleiotropic physiology of SSTs in modulating growth and smoltification. Triploid trout showed significantly down-regulated brain <i>sstr1b1</i> and <i>igfbp2a1</i> (<i>p</i> < 0.05), while diploid trout showed up-regulated brain <i>igfbp1a1</i> (~2.61-fold, <i>p</i> = 0.057) and <i>igfbp2a</i> subtypes (~1.38-fold, <i>p</i> < 0.05), suggesting triploid trout exhibited a better acclimation to the seawater environment. The triploid trout showed up-regulated kidney <i>igfbp5a</i> subtypes (~6.62 and 7.25-fold, <i>p</i> = 0.099 and 0.078) and significantly down-regulated <i>igfbp5b2</i> (~0.37-fold, <i>p</i> < 0.05), showing a conserved physiology of teleost IGFBP5a in regulating osmoregulation. The IGFBP6 subtypes are involved in energy and nutritional regulation. Distinctive <i>igfbp6</i> subtypes patterns (<i>p</i> < 0.05) potentially indicated trout triggered energy redistribution in brain and kidney during osmoregulatory regulation. In conclusion, we showed that the GHRH-SST-GH-IGF axis exhibited pleiotropic effects in regulating growth and osmoregulatory regulation during trout smolting, which might provide new insights into seawater aquaculture of salmonid species.https://www.mdpi.com/1422-0067/23/15/8691triploid rainbow trout<i>ghrh-gh-sst-igf</i> axisosmoregulation
spellingShingle Kaiwen Xiang
Qian Yang
Mengqun Liu
Xiaodong Yang
Jifang Li
Zhishuai Hou
Haishen Wen
Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
International Journal of Molecular Sciences
triploid rainbow trout
<i>ghrh-gh-sst-igf</i> axis
osmoregulation
title Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
title_full Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
title_fullStr Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
title_full_unstemmed Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
title_short Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (<i>Oncorhynchus mykiss</i>)
title_sort crosstalk between growth and osmoregulation of ghrh sst gh igf axis in triploid rainbow trout i oncorhynchus mykiss i
topic triploid rainbow trout
<i>ghrh-gh-sst-igf</i> axis
osmoregulation
url https://www.mdpi.com/1422-0067/23/15/8691
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