Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism

High glycogen in oysters contributes to their flavor, quality, and hardiness, making it a crucial target trait for breeding purposes. Until now, the upstream regulatory mechanism for glycogen synthesis has remained unclear. Protein phosphatase-1 regulatory subunit 3 (PPP1R3) is a member of a family...

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Published in:Aquaculture Reports
Main Authors: Yinchuan Zhang, Jie Meng, Fei Xu
Format: Article in Journal/Newspaper
Language:English
Published: Elsevier 2024
Subjects:
Online Access:https://doi.org/10.1016/j.aqrep.2024.102258
https://doaj.org/article/f49f7e3f008740b19d6d4d231fda91f9
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spelling ftdoajarticles:oai:doaj.org/article:f49f7e3f008740b19d6d4d231fda91f9 2024-09-15T18:03:11+00:00 Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism Yinchuan Zhang Jie Meng Fei Xu 2024-08-01T00:00:00Z https://doi.org/10.1016/j.aqrep.2024.102258 https://doaj.org/article/f49f7e3f008740b19d6d4d231fda91f9 EN eng Elsevier http://www.sciencedirect.com/science/article/pii/S2352513424003466 https://doaj.org/toc/2352-5134 2352-5134 doi:10.1016/j.aqrep.2024.102258 https://doaj.org/article/f49f7e3f008740b19d6d4d231fda91f9 Aquaculture Reports, Vol 37, Iss , Pp 102258- (2024) Molluscan Glycogen PP1/PPP1R3 Overexpression Polymorphism Aquaculture. Fisheries. Angling SH1-691 article 2024 ftdoajarticles https://doi.org/10.1016/j.aqrep.2024.102258 2024-08-26T15:21:18Z High glycogen in oysters contributes to their flavor, quality, and hardiness, making it a crucial target trait for breeding purposes. Until now, the upstream regulatory mechanism for glycogen synthesis has remained unclear. Protein phosphatase-1 regulatory subunit 3 (PPP1R3) is a member of a family that directs the protein phosphatase-1 (PP1) to glycogen, resulting in the activation of glycogen synthase (GS) and the inactivation of glycogen phosphorylase (GP). However, their functions in molluscan species have remained unclear until now. In our study, we verified the function of the PP1α/PPP1R3D pathways in the glycogen metabolism process in Crassostrea gigas. Initially, we conducted a phylogenetic analysis and identified two PP1 and PPP1R3 members in molluscan species, emphasizing copy number variations in eukaryotic animals. Additionally, we identified distinct substitutions of conserved motifs specific to bivalves, Cephalopoda, or Gastropods, revealing functional diversity in PP1 and PPP1R3. Our primary focus was on PP1α/PPP1R3D in the oyster C.gigas, detected in the muscle glycogen fraction of bivalve species, with mRNA expression showing a positive correlation with glycogen content. By manipulating CgPPP1R3D expression in oysters through adenovirus-mediated overexpression or siRNA-mediated downregulation, we established a direct positive correlation between CgPPP1R3D expression levels and glycogen content. Colocation analysis confirmed protein interactions between CgPP1α and CgPPP1R3D. Furthermore, to elucidate the correlation between gene expression and glycogen accumulation, we conducted an association analysis and identified a cluster of significant SNP loci upstream of CgPPP1R3D significantly related to glycogen content. The high polymorphism observed may be linked to differential expressions of CgPPP1R3D in oyster individuals with high and low glycogen levels. These findings serve as a crucial reference for enhancing glycogen traits in molluscan species. Article in Journal/Newspaper Crassostrea gigas Directory of Open Access Journals: DOAJ Articles Aquaculture Reports 37 102258
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Molluscan
Glycogen
PP1/PPP1R3
Overexpression
Polymorphism
Aquaculture. Fisheries. Angling
SH1-691
spellingShingle Molluscan
Glycogen
PP1/PPP1R3
Overexpression
Polymorphism
Aquaculture. Fisheries. Angling
SH1-691
Yinchuan Zhang
Jie Meng
Fei Xu
Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
topic_facet Molluscan
Glycogen
PP1/PPP1R3
Overexpression
Polymorphism
Aquaculture. Fisheries. Angling
SH1-691
description High glycogen in oysters contributes to their flavor, quality, and hardiness, making it a crucial target trait for breeding purposes. Until now, the upstream regulatory mechanism for glycogen synthesis has remained unclear. Protein phosphatase-1 regulatory subunit 3 (PPP1R3) is a member of a family that directs the protein phosphatase-1 (PP1) to glycogen, resulting in the activation of glycogen synthase (GS) and the inactivation of glycogen phosphorylase (GP). However, their functions in molluscan species have remained unclear until now. In our study, we verified the function of the PP1α/PPP1R3D pathways in the glycogen metabolism process in Crassostrea gigas. Initially, we conducted a phylogenetic analysis and identified two PP1 and PPP1R3 members in molluscan species, emphasizing copy number variations in eukaryotic animals. Additionally, we identified distinct substitutions of conserved motifs specific to bivalves, Cephalopoda, or Gastropods, revealing functional diversity in PP1 and PPP1R3. Our primary focus was on PP1α/PPP1R3D in the oyster C.gigas, detected in the muscle glycogen fraction of bivalve species, with mRNA expression showing a positive correlation with glycogen content. By manipulating CgPPP1R3D expression in oysters through adenovirus-mediated overexpression or siRNA-mediated downregulation, we established a direct positive correlation between CgPPP1R3D expression levels and glycogen content. Colocation analysis confirmed protein interactions between CgPP1α and CgPPP1R3D. Furthermore, to elucidate the correlation between gene expression and glycogen accumulation, we conducted an association analysis and identified a cluster of significant SNP loci upstream of CgPPP1R3D significantly related to glycogen content. The high polymorphism observed may be linked to differential expressions of CgPPP1R3D in oyster individuals with high and low glycogen levels. These findings serve as a crucial reference for enhancing glycogen traits in molluscan species.
format Article in Journal/Newspaper
author Yinchuan Zhang
Jie Meng
Fei Xu
author_facet Yinchuan Zhang
Jie Meng
Fei Xu
author_sort Yinchuan Zhang
title Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
title_short Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
title_full Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
title_fullStr Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
title_full_unstemmed Genome-wide identification of the PP1 and PPP1R3 gene family in oyster Crassostrea gigas: Unraveling their roles in glycogen metabolism
title_sort genome-wide identification of the pp1 and ppp1r3 gene family in oyster crassostrea gigas: unraveling their roles in glycogen metabolism
publisher Elsevier
publishDate 2024
url https://doi.org/10.1016/j.aqrep.2024.102258
https://doaj.org/article/f49f7e3f008740b19d6d4d231fda91f9
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source Aquaculture Reports, Vol 37, Iss , Pp 102258- (2024)
op_relation http://www.sciencedirect.com/science/article/pii/S2352513424003466
https://doaj.org/toc/2352-5134
2352-5134
doi:10.1016/j.aqrep.2024.102258
https://doaj.org/article/f49f7e3f008740b19d6d4d231fda91f9
op_doi https://doi.org/10.1016/j.aqrep.2024.102258
container_title Aquaculture Reports
container_volume 37
container_start_page 102258
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