Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc

Spermatogonial cells are capable of transmitting genetic information to the next generation and have the potential for self-renewal. However, research on spermatogonial cells is generally limited by the paucity of cell surface markers, which are not universal among species. In this study, we develop...

Full description

Saved in:
Bibliographic Details
Main Authors: Liangjie Liu, Ya Shu, Tian Liu, Huilan Wei, Yaxin Yang, Lijing Zhang, Xiaohui Ma, Guoqing Li, Yajuan Li, Shi Wang, Lingling Zhang
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Computational and Structural Biotechnology Journal
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2001037025000236
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832582157641449472
author Liangjie Liu
Ya Shu
Tian Liu
Huilan Wei
Yaxin Yang
Lijing Zhang
Xiaohui Ma
Guoqing Li
Yajuan Li
Shi Wang
Lingling Zhang
author_facet Liangjie Liu
Ya Shu
Tian Liu
Huilan Wei
Yaxin Yang
Lijing Zhang
Xiaohui Ma
Guoqing Li
Yajuan Li
Shi Wang
Lingling Zhang
author_sort Liangjie Liu
collection DOAJ
description Spermatogonial cells are capable of transmitting genetic information to the next generation and have the potential for self-renewal. However, research on spermatogonial cells is generally limited by the paucity of cell surface markers, which are not universal among species. In this study, we developed a systematic screening strategy for germline regulatory pathways and spermatogonial surface markers in non-model organisms. This was achieved by combining weighted gene co-expression network analysis (WGCNA), differential expressed gene (DEG) overrepresentation analysis, and functional annotation. This strategy was employed to identify a spermatogonia-related module, which was found to be enriched with stem cell-related pathways in the scallop Patinopecten yessoensis. This module contained a transmembrane protein, fibroblast growth factor receptor (FGFR). A single copy of Fgfr (PyFgfr) was confirmed in the P. yessoensis genome, which exhibited the canonical functional domains of FGFRs. PyFgfr was universally expressed in multiple tissues, including the testis. The highest expression was observed at the resting stage of the testis, with exclusive localization in spermatogonia. To obtain antibodies that recognize the cell surface region, the extracellular domains of PyFGFR were used as an antigen to prepare antiserum. Western blotting, immunohistochemical, and immunofluorescent analyses demonstrated that the antiserum specifically detected PyFGFR in the spermatogonia. This study demonstrates the feasibility of this strategy for screening spermatogonial surface markers in the scallop. This approach will facilitate the culture and manipulation of spermatogonia in non-model organisms, which may contribute to genetic improvement in aquaculture.
format Article
id doaj-art-464b881489de41aaa92af501c43bd0e9
institution Kabale University
issn 2001-0370
language English
publishDate 2025-01-01
publisher Elsevier
record_format Article
series Computational and Structural Biotechnology Journal
spelling doaj-art-464b881489de41aaa92af501c43bd0e92025-01-30T05:13:54ZengElsevierComputational and Structural Biotechnology Journal2001-03702025-01-0127519530Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve molluscLiangjie Liu0Ya Shu1Tian Liu2Huilan Wei3Yaxin Yang4Lijing Zhang5Xiaohui Ma6Guoqing Li7Yajuan Li8Shi Wang9Lingling Zhang10MOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology & Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao 266237, China; Laboratory of Tropical Marine Germplasm Resources and Breeding Engineering, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaMOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology & Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao 266237, China; Corresponding author at: MOE Key Laboratory of Marine Genetics and Breeding, Ocean University of China, Qingdao 266003, China.Spermatogonial cells are capable of transmitting genetic information to the next generation and have the potential for self-renewal. However, research on spermatogonial cells is generally limited by the paucity of cell surface markers, which are not universal among species. In this study, we developed a systematic screening strategy for germline regulatory pathways and spermatogonial surface markers in non-model organisms. This was achieved by combining weighted gene co-expression network analysis (WGCNA), differential expressed gene (DEG) overrepresentation analysis, and functional annotation. This strategy was employed to identify a spermatogonia-related module, which was found to be enriched with stem cell-related pathways in the scallop Patinopecten yessoensis. This module contained a transmembrane protein, fibroblast growth factor receptor (FGFR). A single copy of Fgfr (PyFgfr) was confirmed in the P. yessoensis genome, which exhibited the canonical functional domains of FGFRs. PyFgfr was universally expressed in multiple tissues, including the testis. The highest expression was observed at the resting stage of the testis, with exclusive localization in spermatogonia. To obtain antibodies that recognize the cell surface region, the extracellular domains of PyFGFR were used as an antigen to prepare antiserum. Western blotting, immunohistochemical, and immunofluorescent analyses demonstrated that the antiserum specifically detected PyFGFR in the spermatogonia. This study demonstrates the feasibility of this strategy for screening spermatogonial surface markers in the scallop. This approach will facilitate the culture and manipulation of spermatogonia in non-model organisms, which may contribute to genetic improvement in aquaculture.http://www.sciencedirect.com/science/article/pii/S2001037025000236FgfrSurface markerWGCNASpermatogonial cellsPatinopecten yessoensis
spellingShingle Liangjie Liu
Ya Shu
Tian Liu
Huilan Wei
Yaxin Yang
Lijing Zhang
Xiaohui Ma
Guoqing Li
Yajuan Li
Shi Wang
Lingling Zhang
Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
Computational and Structural Biotechnology Journal
Fgfr
Surface marker
WGCNA
Spermatogonial cells
Patinopecten yessoensis
title Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
title_full Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
title_fullStr Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
title_full_unstemmed Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
title_short Systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
title_sort systematic screening and dynamic profiling of germline regulatory pathways and spermatogonial surface markers in a bivalve mollusc
topic Fgfr
Surface marker
WGCNA
Spermatogonial cells
Patinopecten yessoensis
url http://www.sciencedirect.com/science/article/pii/S2001037025000236
work_keys_str_mv AT liangjieliu systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT yashu systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT tianliu systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT huilanwei systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT yaxinyang systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT lijingzhang systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT xiaohuima systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT guoqingli systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT yajuanli systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT shiwang systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc
AT linglingzhang systematicscreeninganddynamicprofilingofgermlineregulatorypathwaysandspermatogonialsurfacemarkersinabivalvemollusc