Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle
Carotenoids are essential nutrients for humans and animals, and carotenoid content has become an important trait to evaluate the nutritional value of many cultured animals. Marine animals provide humans with diverse carotenoids, and developing carotenoid-enriched varieties has been the focus of mari...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-05-01
|
| Series: | Frontiers in Marine Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2023.1158325/full |
| _version_ | 1797822454448521216 |
|---|---|
| author | Tingting Li Yihan Zhang Shiqi Liu Moli Li Ruixing Yao Senyu Niu Jingyao Yuan Huizhen Wang Huizhen Wang Jingjie Hu Jingjie Hu Zhenmin Bao Zhenmin Bao Zhenmin Bao Xiaoli Hu Xiaoli Hu |
| author_facet | Tingting Li Yihan Zhang Shiqi Liu Moli Li Ruixing Yao Senyu Niu Jingyao Yuan Huizhen Wang Huizhen Wang Jingjie Hu Jingjie Hu Zhenmin Bao Zhenmin Bao Zhenmin Bao Xiaoli Hu Xiaoli Hu |
| author_sort | Tingting Li |
| collection | DOAJ |
| description | Carotenoids are essential nutrients for humans and animals, and carotenoid content has become an important trait to evaluate the nutritional value of many cultured animals. Marine animals provide humans with diverse carotenoids, and developing carotenoid-enriched varieties has been the focus of marine animal breeding. Understanding the molecular mechanism of carotenoid deposition could benefit marine animal breeding for carotenoid content improvement. In the present study, transcriptomic analysis of adductor muscle was performed between Yesso scallop (Patinopecten yessoensis) with white muscle (WM) and carotenoid-enriched orange muscle (OM). A total of 683 differentially expressed genes (DEGs) were identified, with 302 and 381 genes being up- and down-regulated in OM scallop. Gene co-expression network analysis identified four carotenoid accumulation−related modules, including three up-regulated modules and one down-regulated module. The genes in up-regulated modules mainly participate in the pathways of translation and transcription (MEgreen), immune system (MElightyellow), and lipid metabolism (MEpink), while the down-regulated module is mainly enriched with genes involved in various metabolic pathways (MEturquoise). As the causal gene responsible for muscle coloration in scallop, PyBCO-like 1 is the hub gene of MEturquoise and showed strong connectivity with NR2F1A, a transcriptional factor involved in the regulation of retinoic acid. In addition, the up-regulated DEGs, including WDR3, RPP29, TBL3, RIOK2, and NOB1 from “ribosome biogenesis”, HSP70s and HSP702Bs from “antigen processing and presentation”, and ACOX1 from “PPAR signaling pathway” were identified as hub genes, indicating the potential regulatory role of these genes and pathways in response to carotenoid accumulation. Our data contribute to a deeper understanding of the regulatory and response mechanisms of carotenoid accumulation in marine animals. |
| first_indexed | 2024-03-13T10:09:17Z |
| format | Article |
| id | doaj.art-2a5eba2ca60344e880fc5b79771470f7 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-03-13T10:09:17Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-2a5eba2ca60344e880fc5b79771470f72023-05-22T04:55:02ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-05-011010.3389/fmars.2023.11583251158325Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscleTingting Li0Yihan Zhang1Shiqi Liu2Moli Li3Ruixing Yao4Senyu Niu5Jingyao Yuan6Huizhen Wang7Huizhen Wang8Jingjie Hu9Jingjie Hu10Zhenmin Bao11Zhenmin Bao12Zhenmin Bao13Xiaoli Hu14Xiaoli Hu15Ministry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaLaboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya, ChinaMinistry of Education (MOE) Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaCarotenoids are essential nutrients for humans and animals, and carotenoid content has become an important trait to evaluate the nutritional value of many cultured animals. Marine animals provide humans with diverse carotenoids, and developing carotenoid-enriched varieties has been the focus of marine animal breeding. Understanding the molecular mechanism of carotenoid deposition could benefit marine animal breeding for carotenoid content improvement. In the present study, transcriptomic analysis of adductor muscle was performed between Yesso scallop (Patinopecten yessoensis) with white muscle (WM) and carotenoid-enriched orange muscle (OM). A total of 683 differentially expressed genes (DEGs) were identified, with 302 and 381 genes being up- and down-regulated in OM scallop. Gene co-expression network analysis identified four carotenoid accumulation−related modules, including three up-regulated modules and one down-regulated module. The genes in up-regulated modules mainly participate in the pathways of translation and transcription (MEgreen), immune system (MElightyellow), and lipid metabolism (MEpink), while the down-regulated module is mainly enriched with genes involved in various metabolic pathways (MEturquoise). As the causal gene responsible for muscle coloration in scallop, PyBCO-like 1 is the hub gene of MEturquoise and showed strong connectivity with NR2F1A, a transcriptional factor involved in the regulation of retinoic acid. In addition, the up-regulated DEGs, including WDR3, RPP29, TBL3, RIOK2, and NOB1 from “ribosome biogenesis”, HSP70s and HSP702Bs from “antigen processing and presentation”, and ACOX1 from “PPAR signaling pathway” were identified as hub genes, indicating the potential regulatory role of these genes and pathways in response to carotenoid accumulation. Our data contribute to a deeper understanding of the regulatory and response mechanisms of carotenoid accumulation in marine animals.https://www.frontiersin.org/articles/10.3389/fmars.2023.1158325/fullPatinopecten yessoensiscarotenoid accumulationgene co-expression network analysisPyBCO-like 1molecular mechanism |
| spellingShingle | Tingting Li Yihan Zhang Shiqi Liu Moli Li Ruixing Yao Senyu Niu Jingyao Yuan Huizhen Wang Huizhen Wang Jingjie Hu Jingjie Hu Zhenmin Bao Zhenmin Bao Zhenmin Bao Xiaoli Hu Xiaoli Hu Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle Frontiers in Marine Science Patinopecten yessoensis carotenoid accumulation gene co-expression network analysis PyBCO-like 1 molecular mechanism |
| title | Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| title_full | Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| title_fullStr | Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| title_full_unstemmed | Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| title_short | Transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| title_sort | transcriptome and network analyses reveal key pathways and genes involved in response to carotenoid deposition in scallop muscle |
| topic | Patinopecten yessoensis carotenoid accumulation gene co-expression network analysis PyBCO-like 1 molecular mechanism |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2023.1158325/full |
| work_keys_str_mv | AT tingtingli transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT yihanzhang transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT shiqiliu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT molili transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT ruixingyao transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT senyuniu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT jingyaoyuan transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT huizhenwang transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT huizhenwang transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT jingjiehu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT jingjiehu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT zhenminbao transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT zhenminbao transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT zhenminbao transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT xiaolihu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle AT xiaolihu transcriptomeandnetworkanalysesrevealkeypathwaysandgenesinvolvedinresponsetocarotenoiddepositioninscallopmuscle |