Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin <italic style="font-style: italic">Trachidermus</italic> <italic style="font-style: italic">fasciatus</italic>

Dongxiu XUE; Sudong XIA; Tengfei XING; Yuqian GAO; Jinxian LIU

doi:10.1007/s00343-024-3285-8

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Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus

Biology | Updated：2024-11-19

- Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus
- Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus
- 海洋湖沼学报(英文) 2024年42卷第5期页码：1673-1682
- Affiliations：
  
  1.CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao266071, China
  2.Laboratory for Marine Ecology and Environmental Science, Qingdao Marine Science and Technology Center, Qingdao266200, China
  3.Tianjin Key Lab of Aqua-Ecology and Aquaculture, Department of Fishery Science, Tianjin300380, China
- Author bio：
  
  xuedongxiu@qdio.ac.cn
- Funds：
  
  the National Natural Science Foundation of China(31972793;31502169);the Key Scientific Research Project in Universities and Colleges in Tianjin(2022ZD004)
- DOI：10.1007/s00343-024-3285-8
  中图分类号：
- 收稿：2023-12-26，
  
  网络首发：2024-02-18，
  
  纸质出版：2024-09-01
- Accepted：
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Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus[J]. 海洋湖沼学报(英文), 2024,42(5):1673-1682.

XUE Dongxiu,XIA Sudong,XING Tengfei,et al.Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus[J].Journal of Oceanology and Limnology,2024,42(05):1673-1682.
Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus[J]. 海洋湖沼学报(英文), 2024,42(5):1673-1682. DOI： 10.1007/s00343-024-3285-8.

XUE Dongxiu,XIA Sudong,XING Tengfei,et al.Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus[J].Journal of Oceanology and Limnology,2024,42(05):1673-1682. DOI： 10.1007/s00343-024-3285-8.

摘要

Abstract

The mechanisms underlying sex determination and differentiation have long intrigued researchers in the fields of development and evolutionary biology. The roughskin sculpin (

Trachidermus

fasciatus

Heckel)

displaying sexual dimorphism

provides an ideal model for studying the mechanisms. However

both genetic and genomic information concerning sex determination and differentiation

such as gonadal transcriptome data in roughskin sculpin

are lacking. Here

we present the first gonadal transcriptomes of roughskin sculpin and identify sex-related genes. We identified 8 531 differentially expressed genes (DEGs)

among them 4 065 were upregulated in the ovary and 4 466 upregulated in the testis. Several sex-related gene ontology (GO) terms were enriched in ovary-biased genes

including “binding of sperm to zona pellucida”

“egg coat formation”

“positive regulation of acrosome reaction”

“cell division”

and “cell cycle”

while the GO terms such as “spermatogenesis”

“sperm axoneme assembly”

“cilium assembly”

“cilium movement”

and “cilium movement involved in cell motility” were enriched in testis-biased genes. Moreover

six KEGG pathways were significantly enriched in the ovary

whereas only one was enriched in the testis. Of these DEGs

40 sex-related genes were identified

which including 26 testis-biased genes (such as

Dmrtb1

Gsdf

Sox9b

Wnt4b

Tcp11l2

and

Efhb

)

and 14 ovary-biased genes (such as

Cyp19a1a

Foxh1

Foxr1

Gdf3

Hsd17b12

and

Igf2bp3

). This gonadal transcript dataset would broaden our understanding of sex determination and differentiation mechanisms in roughskin sculpin

expand the genomic database

support future studies on sex-related gene functions

and facilitate molecular biology research into roughskin sculpin.

关键词

Keywords

references

Bachtrog D , Mank J E , Peichel C L et al . 2014 . Sex determination: why so many ways of doing it? PLOS Biology , 12 ( 7 ): e1001899 , https://doi.org/10.1371/journal.pbio.1001899 https://doi.org/10.1371/journal.pbio.1001899 .

Bernard P , Harley V R . 2007 . Wnt4 action in gonadal development and sex determination . The International Journal of Biochemistry & Cell Biology , 39 ( 1 ): 31 - 43 , https://doi.org/10.1016/j.biocel.2006.06.007 https://doi.org/10.1016/j.biocel.2006.06.007 .

Chen H P , Li S S , Xiao L et al . 2015 . Wnt4 in protogynous hermaphroditic orange-spotted grouper ( Epinephelus coioides ): identification and expression . Comparative Biochemistry and Physiology Part B : Biochemistry and Molecular Biology , 183 : 67 - 74 , https://doi.‍org/10.1016/j.cbpb.2015.01.002 https://doi.‍org/10.1016/j.cbpb.2015.01.002 . https://do 10.1016/j.cbpb.2015.01.002 http://dx.doi.org/10.1016/j.cbpb.2015.01.002

Chiang E F L , Pai C I , Wyatt M et al . 2001 . Two Sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites . Developmental Biology , 231 ( 1 ): 149 - 163 , https://doi.org/10.1006/dbio.2000.0129 https://doi.org/10.1006/dbio.2000.0129 .

Diotel N , Page Y L , Mouriec K et al . 2010 . Aromatase in the brain of teleost fish: expression, regulation and putative functions . Frontiers in Neuroendocrinology , 31 ( 2 ): 172 - 192 , https://doi.‍org/10.1016/j.yfrne.2010.01.003 https://doi.‍org/10.1016/j.yfrne.2010.01.003 . https://do 10.1016/j.yfrne.2010.01.003 http://dx.doi.org/10.1016/j.yfrne.2010.01.003

Du X X , Wang B , Liu X M et al . 2017 . Comparative transcriptome analysis of ovary and testis reveals potential sex-related genes and pathways in spotted knifejaw Oplegnathus punctatus . Gene , 637 : 203 - 210 , https://doi.org/10.1016/j.gene.2017.09.055 https://doi.org/10.1016/j.gene.2017.09.055 .

Fan Z F , You F , Wang L J et al . 2014 . Gonadal transcriptome analysis of male and female olive flounder ( Paralichthys olivaceus ) . BioMed Research International , 2014 ( 2 ): 291067 , https://doi.org/10.1155/2014/291067 https://doi.org/10.1155/2014/291067 .

Gonen N , Lovell-Badge R . 2019 . Chapter Eight: the regulation of Sox9 expression in the gonad . In: Capel B ed. Current Topics in Developmental Biology . Academic Press , Amsterdam , https://doi.‍org/10.1016/bs.ctdb.2019.01.004 https://doi.‍org/10.1016/bs.ctdb.2019.01.004 . https://do 10.1016/bs.ctdb.2019.01.004 http://dx.doi.org/10.1016/bs.ctdb.2019.01.004

Gong J , Li B J , Zhao J et al . 2022 . Sex-specific genomic region identification and molecular sex marker development of rock bream ( Oplegnathus fasciatus ) . Marine Biotechnology , 24 ( 1 ): 163 - 173 , https://doi.‍org/10.1007/s10126-022-10095-2 https://doi.‍org/10.1007/s10126-022-10095-2 . https://do 10.1007/s10126-022-10095-2 http://dx.doi.org/10.1007/s10126-022-10095-2

Goto A , Yokoyama R , Sideleva V G . 2015 . Evolutionary diversification in freshwater sculpins (Cottoidea): a review of two major adaptive radiations . Environmental Biology of Fishes , 98 ( 1 ): 307 - 335 , https://doi.org/10.1007/s10641-014-0262-7 https://doi.org/10.1007/s10641-014-0262-7 .

Graves J A M . 2016 . Evolution of vertebrate sex chromosomes and dosage compensation . Nature Reviews Genetics , 17 : 33 - 46 , https://doi.‍org/10.1038/nrg.2015.2 https://doi.‍org/10.1038/nrg.2015.2 . https://do 10.1038/nrg.2015.2 http://dx.doi.org/10.1038/nrg.2015.2

Guan W Z , Jiang K , Lai X L et al . 2022 . Comprehens ive transcriptome analysis of gonadal and somatic tissues for identification of sex-related genes in the largemouth bass Micropterus salmoides . Marine Biotechnology , 24 ( 3 ): 588 - 598 , https://doi.org/10.1007/s10126-022-10127-x https://doi.org/10.1007/s10126-022-10127-x .

Guiguen Y , Fostier A , Piferrer F et al . 2010 . Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish . General and Comparative Endocrinology , 165 ( 3 ): 352 - 366 , https://doi.org/10.1016/j.ygcen.2009.03.002 https://doi.org/10.1016/j.ygcen.2009.03.002 .

He F X , Jiang D N , Huang Y Q et al . 2019 . Comparative transcriptome analysis of male and female gonads reveals sex-biased genes in spotted scat ( Scatophagus argus ) . Fish Physiology and Biochemistry , 45 ( 6 ): 1963 - 1980 , https://doi.‍org/10.1007/s10695-019-00693-8 https://doi.‍org/10.1007/s10695-019-00693-8 . https://do 10.1007/s10695-019-00693-8 http://dx.doi.org/10.1007/s10695-019-00693-8

Jakob S , Lovell-Badge R . 2011 . Sex determination and the control of Sox9 expression in mammals . The FEBS Journal , 278 ( 7 ): 1002 - 1009 , https://doi.‍org/10.1111/j.1742-4658.2011.08029.x https://doi.‍org/10.1111/j.1742-4658.2011.08029.x . https://do 10.1111/j.1742-4658.2011.08029.x http://dx.doi.org/10.1111/j.1742-4658.2011.08029.x

Kim D , Langmead B , Salzberg S L et al . 2015 . HISAT: a fast spliced aligner with low memory requirements . Nature Methods , 12 ( 4 ): 357 - 360 , https://doi.‍org/10.1038/nmeth.3317 https://doi.‍org/10.1038/nmeth.3317 . https://do 10.1038/nmeth.3317 http://dx.doi.org/10.1038/nmeth.3317

Kim D , Paggi J M , Park C et al . 2019 . Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype . Nature Biotechnology , 37 ( 8 ): 907 - 915 , https://doi.org/10.1038/s41587-019-0201-4 https://doi.org/10.1038/s41587-019-0201-4 .

Kobayashi Y , Horiguchi R , Miura S et al . 2010 . Sex- and tissue-specific expression of P450 aromatase ( Cyp 19 a 1 a) in the yellowtail clownfish, Amphiprion clarkii . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 155 ( 2 ): 237 - 244 , https://doi.org/10.1016/j.cbpa.2009.11.004 https://doi.org/10.1016/j.cbpa.2009.11.004 .

Kobayashi Y , Nagahama Y , Nakamura M . 2012 . Diversity and plasticity of sex determination and differentiation in fishes . Sexual Development , 7 ( 1-3 ): 115 - 125 , https://doi.org/10.1159/000342009 https://doi.org/10.1159/000342009 .

Kolde R . 2022 . Package 'pheatmap' , Version 1.0.12 , https://cran.ms.unimelb.edu.au/web/packages/pheatmap/pheatmap.pdf https://cran.ms.unimelb.edu.au/web/packages/pheatmap/pheatmap.pdf .

Li H , Handsaker B , Wysoker A et al . 2009 . The sequence alignment/map format and SAMtools . Bioinformatics , 25 ( 16 ): 2078 - 2079 , https://doi.org/10.1093/bioinformatics/btp352 https://doi.org/10.1093/bioinformatics/btp352 .

Li M H , Sun L N , Wang D S . 2019 . Roles of estrogens in fish sexual plasticity and sex differentiation . General and Comparative Endocrinology , 277 : 9 - 16 , https://doi.‍org/10.1016/j.ygcen.2018.11.015 https://doi.‍org/10.1016/j.ygcen.2018.11.015 . https://do 10.1016/j.ygcen.2018.11.015 http://dx.doi.org/10.1016/j.ygcen.2018.11.015

Liu S , Xu P , Liu X G et al . 2021 . Production of neo-male mandarin fish Siniperca chuatsi by masculinization with orally administered 17α-methyltestosterone . Aquaculture , 530 : 735904 , https://doi.‍org/10.1016/j.aquaculture.2020.735904 https://doi.‍org/10.1016/j.aquaculture.2020.735904 . https://do 10.1016/j.aquaculture.2020.735904 http://dx.doi.org/10.1016/j.aquaculture.2020.735904

Love M I , Huber W , Anders S . 2014 . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 . Genome Biology , 15 ( 12 ): 550 , https://doi.org/10.1186/s13059-014-0550-8 https://doi.org/10.1186/s13059-014-0550-8 .

Meyer A , van de Peer Y . 2005 . From 2 R to 3 R: evidence for a fish-specific genome duplication (FSGD). Bioessays, 27 ( 9 ): 937 - 945 , https://doi.org/10.1002/bies.20293 https://doi.org/10.1002/bies.20293 .

Nakamoto M , Suzuki A , Matsuda M et al . 2005 . Testicular type Sox9 is not involved in sex determination but might be in the development of testicular structures in the medaka, Oryzias latipes . Biochemical and Biophysical Research Communications , 333 ( 3 ): 729 - 736 , https://doi.org/10.1016/j.bbrc.2005.05.158 https://doi.org/10.1016/j.bbrc.2005.05.158 .

Nicol B , Guerin A , Fostier A et al . 2012 . Ovary-predominant wnt4 expression during gonadal differentiation is not conserved in the rainbow trout ( Oncorhynchus mykiss ) . Molecular Reproduction & Development , 79 ( 1 ): 51 - 63 , https://doi.org/10.1002/mrd.21404 https://doi.org/10.1002/mrd.21404 .

Onikura N , Takeshita N , Matsui S et al . 2002 . Spawning grounds and nests of Trachidermus fasciatus (Cottidae) in the Kashima and Shiota estuaries system facing Ariake Bay, Japan . Ichthyological Research , 49 ( 2 ): 198 - 201 . https://doi.org/10.1007/s102280200027 https://doi.org/10.1007/s102280200027 .

Oshima Y , Hayashi T , Tokunaga S et al . 2005 . Wnt4 expression in the differentiating gonad of the frog Rana rugosa . Zoological Science , 22 ( 6 ): 689 - 693 , https://doi.org/10.2108/zsj.22.689 https://doi.org/10.2108/zsj.22.689 .

Paixão R V , Silva G F , Caetano A R et al . 2022 . Phylogenomic and expression analysis of Colossoma macropomum cyp 19 a 1 a and cyp 19 a 1 b and their non-classical role in tambaqui sex differentiation. Gene, 843 : 146795 , https://doi‍.org/10.1016/j.gene.2022.146795 https://doi‍.org/10.1016/j.gene.2022.146795 .

Pertea M , Pertea G M , Antonescu C M et al . 2015 . StringTie enables improved reconstruction of a transcriptome from RNA-seq reads . Nature Biotechnology , 33 ( 3 ): 290 - 295 , https://doi.org/10.1038/nbt.3122 https://doi.org/10.1038/nbt.3122 .

Rajendiran P , Jaafar F , Kar S et al . 2021 . Sex determination and differentiation in teleost: roles of genetics, environment, and brain . Biology , 10 ( 10 ): 973 , https://doi.‍org/10.3390/biology10100973 https://doi.‍org/10.3390/biology10100973 . https://do 10.3390/biology10100973 http://dx.doi.org/10.3390/biology10100973

Ramos L , Antunes A . 2022 . Decoding sex: elucidating sex determination and how high-quality genome assemblies are untangling the evolutionary dynamics of sex chromosomes . Genomics , 114 ( 2 ): 110277 , https://doi.org/10.1016/j.ygeno.2022.110277 https://doi.org/10.1016/j.ygeno.2022.110277 .

Shao B X , Tang Z Y , Sun G Y et al . 1980 . On the breeding habit of Trachidermus fasciatus Heckel . Journal of Fisheries of China , 1 : 81 - 86 . (in Chinese with English abstract)

The Tree of Sex Consortium . 2014 . Tree of Sex: A database of sexual systems . Scientific Data , 1 ( 1 ): 140015 , https://doi.org/10.1038/sdata.2014.15 https://doi.org/10.1038/sdata.2014.15 .

Vu V Q , Friendly M , Tavadyan A , 2024 . Package 'ggbiplot' , Version 0.6.2, https://pbil.univ-lyon1.fr/CRAN/web/packages/ggbiplot/ggbiplot.pdf https://pbil.univ-lyon1.fr/CRAN/web/packages/ggbiplot/ggbiplot.pdf .

Wagner G P , Kin K , Lynch V J . 2012 . Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples . Theory in Biosciences , 131 ( 4 ): 281 - 285 , https://doi.org/10.1007/s12064-012-0162-3 https://doi.org/10.1007/s12064-012-0162-3 .

Wang J Q . 1999 . Advances in studies on the ecology and reproductive biology of Trachidermus fasciatus Heckel . Acta Hydrobiologica Sinica , 23 ( 6 ): 729 - 734 , https://doi.org/cnki:sun:sswx.0.1999-06-028. https://doi.org/cnki:sun:sswx.0.1999-06-028. (in Chinese with English abstract)

Wei L , Yang C , Tao W J et al . 2016 . Genome-wide identification and transcriptome-based expression profiling of the Sox gene family in the Nile tilapia ( Oreochromis niloticus ) . International Journal of Molecular Sciences , 17 ( 3 ): 270 , https://doi.org/10.3390/ijms17030270 https://doi.org/10.3390/ijms17030270 .

Wei W Y , Gong Y , Guo X F et al . 2023 . Gonadal transcriptomes reveal sex-biased expression genes associated with sex deter mination and differentiation in red-tail catfish ( Hemibagrus wyckioides ) . BMC Genomics , 24 : 183 , https://doi.org/10.1186/s12864-023-09264-x https://doi.org/10.1186/s12864-023-09264-x .

Weng S D , You F , Fan Z F et al . 2016 . Molecular cloning and sexually dimorphic expression of wnt4 in olive flounder ( Paralichthys olivaceus ) . Fish Physiology and Biochemistry , 42 ( 4 ): 1167 - 1176 , https://doi.‍org/10.1007/s10695-016-0206-6 https://doi.‍org/10.1007/s10695-016-0206-6 . https://do 10.1007/s10695-016-0206-6 http://dx.doi.org/10.1007/s10695-016-0206-6

Wu G C , Chang C F . 2009 . Wnt4 is associated with the development of ovarian tissue in the protandrous black porgy, Acanthopagrus schlegeli . Biology of Reproduction , 81 ( 6 ): 1073 - 1082 , https://doi.org/10.1095/biolreprod.109.077362 https://doi.org/10.1095/biolreprod.109.077362 .

Xue D X , Xing T F , Liu J X . 2022 . A high-quality chromosome-level genome of the endangered roughskin sculpin provides insights into its evolution and adaptation . Molecular Ecology Resources , 22 ( 5 ): 1892 - 1905 , https://doi.org/10.1111/1755-0998.13582 https://doi.org/10.1111/1755-0998.13582 .

Yin Y K , Tang H P , Liu Y et al . 2017 . Targeted disruption of aromatase reveals dual functions of Cyp 19 a 1 a during sex differentiation in zebrafish. Endocrinology , 158 ( 9 ): 3030 - 3041 , https://doi.org/10.1210/en.2016-1865 https://doi.org/10.1210/en.2016-1865 .

Zhang W , Liu Y Z , Yu H Y et al . 2016 . Transcriptome analysis of the gonads of olive flounder ( Paralichthys olivaceus ) . Fish Physiology and Biochemistry , 42 ( 6 ): 1581 - 1594 , https://doi.org/10.1007/s10695-016-0242-2 https://doi.org/10.1007/s10695-016-0242-2 .

Zhao Y J , Zhang M Z , Wen H S . 2013 . Histological Observation of gonad development in Trachidermus fasciatus . Transactions of Oceanology and Limnology , ( 1 ): 16 - 22 , https://doi.org/10.13984/j.cnki.cn37-1141.2013.01.003. https://doi.org/10.13984/j.cnki.cn37-1141.2013.01.003. (in Chinese with English abstract)

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Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus

Comparative transcriptomic analysis of ovary and testis reveals sex-related genes in roughskin sculpin Trachidermus fasciatus

DOI：10.1007/s00343-024-3285-8

摘要

Abstract

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