Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia
Embryonic temperature has a lasting impact on muscle phenotype in vertebrates, involving complex molecular mechanisms that encompass both protein-coding and non-coding genes. Circular RNAs (circRNAs) are a class of regulatory RNAs that play important roles in various biological processes, but the ef...
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Frontiers Media S.A.
2024-08-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2024.1369758/full |
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| author | Golam Rbbani Riaz Murshed Prabhugouda Siriyappagouder Fedor Sharko Fedor Sharko Artem Nedoluzhko Rajesh Joshi Jorge Galindo-Villegas Joost A. M. Raeymaekers Jorge M. O. Fernandes Jorge M. O. Fernandes |
| author_facet | Golam Rbbani Riaz Murshed Prabhugouda Siriyappagouder Fedor Sharko Fedor Sharko Artem Nedoluzhko Rajesh Joshi Jorge Galindo-Villegas Joost A. M. Raeymaekers Jorge M. O. Fernandes Jorge M. O. Fernandes |
| author_sort | Golam Rbbani |
| collection | DOAJ |
| description | Embryonic temperature has a lasting impact on muscle phenotype in vertebrates, involving complex molecular mechanisms that encompass both protein-coding and non-coding genes. Circular RNAs (circRNAs) are a class of regulatory RNAs that play important roles in various biological processes, but the effect of variable thermal conditions on the circRNA transcriptome and its long-term impact on muscle growth plasticity remains largely unexplored. To fill this knowledge gap, we performed a transcriptomic analysis of circRNAs in fast muscle of Nile tilapia (Oreochromis niloticus) subjected to different embryonic temperatures (24°C, 28°C and 32°C) and then reared at a common temperature (28°C) for 4 months. Nile tilapia embryos exhibited faster development and subsequently higher long-term growth at 32°C compared to those reared at 28°C and 24°C. Next-generation sequencing data revealed a total of 5,141 unique circRNAs across all temperature groups, of which 1,604, 1,531, and 1,169 circRNAs were exclusively found in the 24°C, 28°C and 32°C groups, respectively. Among them, circNexn exhibited a 1.7-fold (log2) upregulation in the 24°C group and a 1.3-fold (log2) upregulation in the 32°C group when compared to the 28°C group. Conversely, circTTN and circTTN_b were downregulated in the 24°C groups compared to their 28°C and 32°C counterparts. Furthermore, these differentially expressed circRNAs were found to have multiple interactions with myomiRs, highlighting their potential as promising candidates for further investigation in the context of muscle growth plasticity. Taken together, our findings provide new insights into the molecular mechanisms that may underlie muscle growth plasticity in response to thermal variation in fish, with important implications in the context of climate change, fisheries and aquaculture. |
| format | Article |
| id | doaj-art-e8d99e53bf5d4272aaa17e6951bcfc69 |
| institution | OA Journals |
| issn | 2296-634X |
| language | English |
| publishDate | 2024-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj-art-e8d99e53bf5d4272aaa17e6951bcfc692025-08-20T02:19:07ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-08-011210.3389/fcell.2024.13697581369758Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapiaGolam Rbbani0Riaz Murshed1Prabhugouda Siriyappagouder2Fedor Sharko3Fedor Sharko4Artem Nedoluzhko5Rajesh Joshi6Jorge Galindo-Villegas7Joost A. M. Raeymaekers8Jorge M. O. Fernandes9Jorge M. O. Fernandes10Genomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayGenomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayGenomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayPaleogenomics Laboratory, European University at Saint Petersburg, Saint Petersburg, RussiaPaleogenomics Laboratory, National Research Center “Kurchatov Institute”, Moscow, RussiaPaleogenomics Laboratory, European University at Saint Petersburg, Saint Petersburg, RussiaGenoMar Genetics AS, Oslo, NorwayGenomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayGenomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayGenomics Division, Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayInstitute of Marine Sciences, Spanish National Research Council, Barcelona, SpainEmbryonic temperature has a lasting impact on muscle phenotype in vertebrates, involving complex molecular mechanisms that encompass both protein-coding and non-coding genes. Circular RNAs (circRNAs) are a class of regulatory RNAs that play important roles in various biological processes, but the effect of variable thermal conditions on the circRNA transcriptome and its long-term impact on muscle growth plasticity remains largely unexplored. To fill this knowledge gap, we performed a transcriptomic analysis of circRNAs in fast muscle of Nile tilapia (Oreochromis niloticus) subjected to different embryonic temperatures (24°C, 28°C and 32°C) and then reared at a common temperature (28°C) for 4 months. Nile tilapia embryos exhibited faster development and subsequently higher long-term growth at 32°C compared to those reared at 28°C and 24°C. Next-generation sequencing data revealed a total of 5,141 unique circRNAs across all temperature groups, of which 1,604, 1,531, and 1,169 circRNAs were exclusively found in the 24°C, 28°C and 32°C groups, respectively. Among them, circNexn exhibited a 1.7-fold (log2) upregulation in the 24°C group and a 1.3-fold (log2) upregulation in the 32°C group when compared to the 28°C group. Conversely, circTTN and circTTN_b were downregulated in the 24°C groups compared to their 28°C and 32°C counterparts. Furthermore, these differentially expressed circRNAs were found to have multiple interactions with myomiRs, highlighting their potential as promising candidates for further investigation in the context of muscle growth plasticity. Taken together, our findings provide new insights into the molecular mechanisms that may underlie muscle growth plasticity in response to thermal variation in fish, with important implications in the context of climate change, fisheries and aquaculture.https://www.frontiersin.org/articles/10.3389/fcell.2024.1369758/fulldevelopmental plasticitythermal plasticitynon-coding RNAsmyogenesissomatic growthaquaculture |
| spellingShingle | Golam Rbbani Riaz Murshed Prabhugouda Siriyappagouder Fedor Sharko Fedor Sharko Artem Nedoluzhko Rajesh Joshi Jorge Galindo-Villegas Joost A. M. Raeymaekers Jorge M. O. Fernandes Jorge M. O. Fernandes Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia Frontiers in Cell and Developmental Biology developmental plasticity thermal plasticity non-coding RNAs myogenesis somatic growth aquaculture |
| title | Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia |
| title_full | Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia |
| title_fullStr | Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia |
| title_full_unstemmed | Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia |
| title_short | Embryonic temperature has long-term effects on muscle circRNA expression and somatic growth in Nile tilapia |
| title_sort | embryonic temperature has long term effects on muscle circrna expression and somatic growth in nile tilapia |
| topic | developmental plasticity thermal plasticity non-coding RNAs myogenesis somatic growth aquaculture |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2024.1369758/full |
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