Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis

Romeo, Carlos - Trovero Martínez, María Fernanda - Radío, Santiago - Smircich, Pablo - Rodríguez-Casuriaga, Rosana - Geisinger Wschebor, Adriana - Sotelo-Silveira, José Roberto

Resumen:

Background: Mammalian testis is a highly complex and heterogeneous tissue. This complexity, which mostly derives from spermatogenic cells, is reflected at the transcriptional level, with the largest number of tissue-specific genes and long noncoding RNAs (lncRNAs) compared to other tissues, and one of the highest rates of alternative splicing. Although it is known that adequate alternative-splicing patterns and stage-specific isoforms are critical for successful spermatogenesis, so far only a very limited number of reports have addressed a detailed study of alternative splicing and isoforms along the different spermatogenic stages. Results: In the present work, using highly purified stage-specific testicular cell populations, we detected 33,002 transcripts expressed throughout mouse spermatogenesis not annotated so far. These include both splice variants of already annotated genes, and of hitherto unannotated genes. Using conservative criteria, we uncovered 13,471 spermatogenic lncRNAs, which reflects the still incomplete annotation of lncRNAs. A distinctive feature of lncRNAs was their lower number of splice variants compared to protein-coding ones, adding to the conclusion that lncRNAs are, in general, less complex than mRNAs. Besides, we identified 2,794 unannotated transcripts with high coding potential (including some arising from yet unannotated genes), many of which encode unnoticed putative testisspecific proteins. Some of the most interesting coding splice variants were chosen, and validated through RT-PCR. Remarkably, the largest number of stage-specific unannotated transcripts are expressed during early meiotic prophase stages, whose study has been scarcely addressed in former transcriptomic analyses. Conclusions: We detected a high number of yet unannotated genes and alternatively spliced transcripts along mouse spermatogenesis, hence showing that the transcriptomic diversity of the testis is considerably higher than previously reported. This is especially prominent for specific, underrepresented stages such as those of early meiotic prophase, and its unveiling may constitute a step towards the understanding of their key events.

Detalles Bibliográficos
2024
ANII: FCE_1_2021_1_166510
Spermatogenesis
Transcriptome
Alternative splicing
lncRNAs
Testi
Inglés
Universidad de la República
COLIBRI
https://hdl.handle.net/20.500.12008/49627
Acceso abierto
Licencia Creative Commons Atribución (CC - By 4.0)
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author Romeo, Carlos
author2 Trovero Martínez, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger Wschebor, Adriana
Sotelo-Silveira, José Roberto
author2_role author
author
author
author
author
author
author_facet Romeo, Carlos
Trovero Martínez, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger Wschebor, Adriana
Sotelo-Silveira, José Roberto
author_role author
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collection COLIBRI
dc.contributor.filiacion.none.fl_str_mv Romeo Carlos, IIBCE
Trovero Martínez María Fernanda, IIBCE
Radío Santiago, IIBCE
Smircich Pablo, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Rodríguez-Casuriaga Rosana, IIBCE
Geisinger Wschebor Adriana, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Sotelo-Silveira José Roberto, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
dc.creator.none.fl_str_mv Romeo, Carlos
Trovero Martínez, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger Wschebor, Adriana
Sotelo-Silveira, José Roberto
dc.date.accessioned.none.fl_str_mv 2025-04-07T14:56:37Z
dc.date.available.none.fl_str_mv 2025-04-07T14:56:37Z
dc.date.issued.none.fl_str_mv 2024
dc.description.abstract.none.fl_txt_mv Background: Mammalian testis is a highly complex and heterogeneous tissue. This complexity, which mostly derives from spermatogenic cells, is reflected at the transcriptional level, with the largest number of tissue-specific genes and long noncoding RNAs (lncRNAs) compared to other tissues, and one of the highest rates of alternative splicing. Although it is known that adequate alternative-splicing patterns and stage-specific isoforms are critical for successful spermatogenesis, so far only a very limited number of reports have addressed a detailed study of alternative splicing and isoforms along the different spermatogenic stages. Results: In the present work, using highly purified stage-specific testicular cell populations, we detected 33,002 transcripts expressed throughout mouse spermatogenesis not annotated so far. These include both splice variants of already annotated genes, and of hitherto unannotated genes. Using conservative criteria, we uncovered 13,471 spermatogenic lncRNAs, which reflects the still incomplete annotation of lncRNAs. A distinctive feature of lncRNAs was their lower number of splice variants compared to protein-coding ones, adding to the conclusion that lncRNAs are, in general, less complex than mRNAs. Besides, we identified 2,794 unannotated transcripts with high coding potential (including some arising from yet unannotated genes), many of which encode unnoticed putative testisspecific proteins. Some of the most interesting coding splice variants were chosen, and validated through RT-PCR. Remarkably, the largest number of stage-specific unannotated transcripts are expressed during early meiotic prophase stages, whose study has been scarcely addressed in former transcriptomic analyses. Conclusions: We detected a high number of yet unannotated genes and alternatively spliced transcripts along mouse spermatogenesis, hence showing that the transcriptomic diversity of the testis is considerably higher than previously reported. This is especially prominent for specific, underrepresented stages such as those of early meiotic prophase, and its unveiling may constitute a step towards the understanding of their key events.
dc.description.es.fl_txt_mv Datos disponibles en: https://www.ncbi.nlm.nih.gov/sra/?term=PRJNA548952
dc.description.sponsorship.none.fl_txt_mv ANII: FCE_1_2021_1_166510
dc.format.extent.es.fl_str_mv 17 h
dc.format.mimetype.es.fl_str_mv application/pdf
dc.identifier.citation.es.fl_str_mv Romeo, C, Trovero Martínez, M, Radío, S [y otros autores]. "Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis". BMC Genomics. [en línea] 2024, 25: 295. 17 h. DOI: 10.1186/s12864-024-10170-z
dc.identifier.doi.none.fl_str_mv 10.1186/s12864-024-10170-z
dc.identifier.issn.none.fl_str_mv 1471-2164
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12008/49627
dc.language.iso.none.fl_str_mv en
eng
dc.publisher.es.fl_str_mv Springer
dc.relation.none.fl_str_mv BMC Genomics, 2024, 25: 295.
dc.rights.license.none.fl_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.none.fl_str_mv reponame:COLIBRI
instname:Universidad de la República
instacron:Universidad de la República
dc.subject.es.fl_str_mv Spermatogenesis
Transcriptome
Alternative splicing
lncRNAs
Testi
dc.title.none.fl_str_mv Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
dc.type.es.fl_str_mv Artículo
dc.type.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description Datos disponibles en: https://www.ncbi.nlm.nih.gov/sra/?term=PRJNA548952
eu_rights_str_mv openAccess
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identifier_str_mv Romeo, C, Trovero Martínez, M, Radío, S [y otros autores]. "Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis". BMC Genomics. [en línea] 2024, 25: 295. 17 h. DOI: 10.1186/s12864-024-10170-z
1471-2164
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instacron_str Universidad de la República
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publishDate 2024
reponame_str COLIBRI
repository.mail.fl_str_mv karina.camps@seciu.edu.uy
repository.name.fl_str_mv COLIBRI - Universidad de la República
repository_id_str 4771
rights_invalid_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
spelling Romeo Carlos, IIBCETrovero Martínez María Fernanda, IIBCERadío Santiago, IIBCESmircich Pablo, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Rodríguez-Casuriaga Rosana, IIBCEGeisinger Wschebor Adriana, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Sotelo-Silveira José Roberto, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.2025-04-07T14:56:37Z2025-04-07T14:56:37Z2024Romeo, C, Trovero Martínez, M, Radío, S [y otros autores]. "Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis". BMC Genomics. [en línea] 2024, 25: 295. 17 h. DOI: 10.1186/s12864-024-10170-z1471-2164https://hdl.handle.net/20.500.12008/4962710.1186/s12864-024-10170-zDatos disponibles en: https://www.ncbi.nlm.nih.gov/sra/?term=PRJNA548952Background: Mammalian testis is a highly complex and heterogeneous tissue. This complexity, which mostly derives from spermatogenic cells, is reflected at the transcriptional level, with the largest number of tissue-specific genes and long noncoding RNAs (lncRNAs) compared to other tissues, and one of the highest rates of alternative splicing. Although it is known that adequate alternative-splicing patterns and stage-specific isoforms are critical for successful spermatogenesis, so far only a very limited number of reports have addressed a detailed study of alternative splicing and isoforms along the different spermatogenic stages. Results: In the present work, using highly purified stage-specific testicular cell populations, we detected 33,002 transcripts expressed throughout mouse spermatogenesis not annotated so far. These include both splice variants of already annotated genes, and of hitherto unannotated genes. Using conservative criteria, we uncovered 13,471 spermatogenic lncRNAs, which reflects the still incomplete annotation of lncRNAs. A distinctive feature of lncRNAs was their lower number of splice variants compared to protein-coding ones, adding to the conclusion that lncRNAs are, in general, less complex than mRNAs. Besides, we identified 2,794 unannotated transcripts with high coding potential (including some arising from yet unannotated genes), many of which encode unnoticed putative testisspecific proteins. Some of the most interesting coding splice variants were chosen, and validated through RT-PCR. Remarkably, the largest number of stage-specific unannotated transcripts are expressed during early meiotic prophase stages, whose study has been scarcely addressed in former transcriptomic analyses. Conclusions: We detected a high number of yet unannotated genes and alternatively spliced transcripts along mouse spermatogenesis, hence showing that the transcriptomic diversity of the testis is considerably higher than previously reported. This is especially prominent for specific, underrepresented stages such as those of early meiotic prophase, and its unveiling may constitute a step towards the understanding of their key events.Submitted by Pintos Natalia (nataliapintosmvd@gmail.com) on 2025-04-07T13:51:16Z No. of bitstreams: 2 license_rdf: 24942 bytes, checksum: 58cb336ce230a47d2f88ad02838a665f (MD5) 10.1186-s12864-024-10170-z.pdf: 3982559 bytes, checksum: 23f17ed3037eae76f02b97cad763f682 (MD5)Approved for entry into archive by Faget Cecilia (lfaget@fcien.edu.uy) on 2025-04-07T14:17:51Z (GMT) No. of bitstreams: 2 license_rdf: 24942 bytes, checksum: 58cb336ce230a47d2f88ad02838a665f (MD5) 10.1186-s12864-024-10170-z.pdf: 3982559 bytes, checksum: 23f17ed3037eae76f02b97cad763f682 (MD5)Made available in DSpace by Luna Fabiana (fabiana.luna@seciu.edu.uy) on 2025-04-07T14:56:37Z (GMT). No. of bitstreams: 2 license_rdf: 24942 bytes, checksum: 58cb336ce230a47d2f88ad02838a665f (MD5) 10.1186-s12864-024-10170-z.pdf: 3982559 bytes, checksum: 23f17ed3037eae76f02b97cad763f682 (MD5) Previous issue date: 2024ANII: FCE_1_2021_1_16651017 happlication/pdfenengSpringerBMC Genomics, 2024, 25: 295.Las obras depositadas en el Repositorio se rigen por la Ordenanza de los Derechos de la Propiedad Intelectual de la Universidad de la República.(Res. Nº 91 de C.D.C. de 8/III/1994 – D.O. 7/IV/1994) y por la Ordenanza del Repositorio Abierto de la Universidad de la República (Res. Nº 16 de C.D.C. de 07/10/2014)info:eu-repo/semantics/openAccessLicencia Creative Commons Atribución (CC - By 4.0)SpermatogenesisTranscriptomeAlternative splicinglncRNAsTestiUncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesisArtículoinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionreponame:COLIBRIinstname:Universidad de la Repúblicainstacron:Universidad de la RepúblicaRomeo, CarlosTrovero Martínez, María FernandaRadío, SantiagoSmircich, PabloRodríguez-Casuriaga, RosanaGeisinger Wschebor, AdrianaSotelo-Silveira, José RobertoLICENSElicense.txtlicense.txttext/plain; charset=utf-84267http://localhost:8080/xmlui/bitstream/20.500.12008/49627/5/license.txt6429389a7df7277b72b7924fdc7d47a9MD55CC-LICENSElicense_urllicense_urltext/plain; charset=utf-844http://localhost:8080/xmlui/bitstream/20.500.12008/49627/2/license_urla0ebbeafb9d2ec7cbb19d7137ebc392cMD52license_textlicense_texttext/html; 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públicahttps://udelar.edu.uy/https://www.colibri.udelar.edu.uy/oai/requestkarina.camps@seciu.edu.uyUruguayopendoar:47712025-09-30T18:21:17COLIBRI - Universidad de la Repúblicafalse
spellingShingle Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
Romeo, Carlos
Spermatogenesis
Transcriptome
Alternative splicing
lncRNAs
Testi
status_str publishedVersion
title Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
title_full Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
title_fullStr Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
title_full_unstemmed Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
title_short Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
title_sort Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
topic Spermatogenesis
Transcriptome
Alternative splicing
lncRNAs
Testi
url https://hdl.handle.net/20.500.12008/49627