Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

Abstract Background Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ ce...

Full description

Bibliographic Details
Main Authors: Kleppe, Lene, Edvardsen, Rolf, Furmanek, Tomasz, Andersson, Eva, Skaftnesmo, Kai, Segafredo, Frida Thyri, Wargelius, Anna
Format: Article in Journal/Newspaper
Language:unknown
Published: figshare 2020
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.4837938.v1
https://springernature.figshare.com/collections/Transcriptomic_analysis_of_dead_end_knockout_testis_reveals_germ_cell_and_gonadal_somatic_factors_in_Atlantic_salmon/4837938/1
id ftdatacite:10.6084/m9.figshare.c.4837938.v1
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.4837938.v1 2023-05-15T15:32:21+02:00 Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon Kleppe, Lene Edvardsen, Rolf Furmanek, Tomasz Andersson, Eva Skaftnesmo, Kai Segafredo, Frida Thyri Wargelius, Anna 2020 https://dx.doi.org/10.6084/m9.figshare.c.4837938.v1 https://springernature.figshare.com/collections/Transcriptomic_analysis_of_dead_end_knockout_testis_reveals_germ_cell_and_gonadal_somatic_factors_in_Atlantic_salmon/4837938/1 unknown figshare https://dx.doi.org/10.1186/s12864-020-6513-4 https://dx.doi.org/10.6084/m9.figshare.c.4837938 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Cell Biology Genetics FOS Biological sciences Molecular Biology 39999 Chemical Sciences not elsewhere classified FOS Chemical sciences Immunology FOS Clinical medicine 69999 Biological Sciences not elsewhere classified Developmental Biology Inorganic Chemistry Computational Biology Collection article 2020 ftdatacite https://doi.org/10.6084/m9.figshare.c.4837938.v1 https://doi.org/10.1186/s12864-020-6513-4 https://doi.org/10.6084/m9.figshare.c.4837938 2021-11-05T12:55:41Z Abstract Background Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ cell-specific dead end (dnd). Several approaches may be applied to inhibit Dnd function, including gene knockout, knockdown or immunization. Since it is challenging to develop a successful treatment against a gene product already existing in the body, alternative targets are being explored. Germ cells are surrounded by, and dependent on, gonadal somatic cells. Targeting genes essential for the survival of gonadal somatic cells may be good alternative targets for sterility treatments. Our aim was to identify and characterize novel germ cell and gonadal somatic factors in Atlantic salmon. Results We have for the first time analysed RNA-sequencing data from germ cell-free (GCF)/dnd knockout and wild type (WT) salmon testis and searched for genes preferentially expressed in either germ cells or gonadal somatic cells. To exclude genes with extra-gonadal expression, our dataset was merged with available multi-tissue transcriptome data. We identified 389 gonad specific genes, of which 194 were preferentially expressed within germ cells, and 11 were confined to gonadal somatic cells. Interestingly, 5 of the 11 gonadal somatic transcripts represented genes encoding secreted TGF-β factors; gsdf, inha, nodal and two bmp6-like genes, all representative vaccine targets. Of these, gsdf and inha had the highest transcript levels. Expression of gsdf and inha was further confirmed to be gonad specific, and their spatial expression was restricted to granulosa and Sertoli cells of the ovary and testis, respectively. Finally, we show that inha expression increases with puberty in both ovary and testis tissue, while gsdf expression does not change or decreases during puberty in ovary and testis tissue, respectively. Conclusions This study contributes with transcriptome data on salmon testis tissue with and without germ cells. We provide a list of novel and known germ cell- and gonad somatic specific transcripts, and show that the expression of two highly active gonadal somatic secreted TGF-β factors, gsdf and inha, are located within granulosa and Sertoli cells. Article in Journal/Newspaper Atlantic salmon DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
39999 Chemical Sciences not elsewhere classified
FOS Chemical sciences
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
Computational Biology
spellingShingle Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
39999 Chemical Sciences not elsewhere classified
FOS Chemical sciences
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
Computational Biology
Kleppe, Lene
Edvardsen, Rolf
Furmanek, Tomasz
Andersson, Eva
Skaftnesmo, Kai
Segafredo, Frida Thyri
Wargelius, Anna
Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
topic_facet Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
39999 Chemical Sciences not elsewhere classified
FOS Chemical sciences
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Developmental Biology
Inorganic Chemistry
Computational Biology
description Abstract Background Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ cell-specific dead end (dnd). Several approaches may be applied to inhibit Dnd function, including gene knockout, knockdown or immunization. Since it is challenging to develop a successful treatment against a gene product already existing in the body, alternative targets are being explored. Germ cells are surrounded by, and dependent on, gonadal somatic cells. Targeting genes essential for the survival of gonadal somatic cells may be good alternative targets for sterility treatments. Our aim was to identify and characterize novel germ cell and gonadal somatic factors in Atlantic salmon. Results We have for the first time analysed RNA-sequencing data from germ cell-free (GCF)/dnd knockout and wild type (WT) salmon testis and searched for genes preferentially expressed in either germ cells or gonadal somatic cells. To exclude genes with extra-gonadal expression, our dataset was merged with available multi-tissue transcriptome data. We identified 389 gonad specific genes, of which 194 were preferentially expressed within germ cells, and 11 were confined to gonadal somatic cells. Interestingly, 5 of the 11 gonadal somatic transcripts represented genes encoding secreted TGF-β factors; gsdf, inha, nodal and two bmp6-like genes, all representative vaccine targets. Of these, gsdf and inha had the highest transcript levels. Expression of gsdf and inha was further confirmed to be gonad specific, and their spatial expression was restricted to granulosa and Sertoli cells of the ovary and testis, respectively. Finally, we show that inha expression increases with puberty in both ovary and testis tissue, while gsdf expression does not change or decreases during puberty in ovary and testis tissue, respectively. Conclusions This study contributes with transcriptome data on salmon testis tissue with and without germ cells. We provide a list of novel and known germ cell- and gonad somatic specific transcripts, and show that the expression of two highly active gonadal somatic secreted TGF-β factors, gsdf and inha, are located within granulosa and Sertoli cells.
format Article in Journal/Newspaper
author Kleppe, Lene
Edvardsen, Rolf
Furmanek, Tomasz
Andersson, Eva
Skaftnesmo, Kai
Segafredo, Frida Thyri
Wargelius, Anna
author_facet Kleppe, Lene
Edvardsen, Rolf
Furmanek, Tomasz
Andersson, Eva
Skaftnesmo, Kai
Segafredo, Frida Thyri
Wargelius, Anna
author_sort Kleppe, Lene
title Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
title_short Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
title_full Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
title_fullStr Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
title_full_unstemmed Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon
title_sort transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in atlantic salmon
publisher figshare
publishDate 2020
url https://dx.doi.org/10.6084/m9.figshare.c.4837938.v1
https://springernature.figshare.com/collections/Transcriptomic_analysis_of_dead_end_knockout_testis_reveals_germ_cell_and_gonadal_somatic_factors_in_Atlantic_salmon/4837938/1
genre Atlantic salmon
genre_facet Atlantic salmon
op_relation https://dx.doi.org/10.1186/s12864-020-6513-4
https://dx.doi.org/10.6084/m9.figshare.c.4837938
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.4837938.v1
https://doi.org/10.1186/s12864-020-6513-4
https://doi.org/10.6084/m9.figshare.c.4837938
_version_ 1766362866438373376