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

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

Resumen:

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
Agencia Nacional de Investigación e Innovación
Comisión Sectorial Investigación Científica (CSIC, UdelaR)
meiosis
spermatogenesis
transcriptomics
alternative splicing
lncRNAs
Ciencias Naturales y Exactas
Ciencias Biológicas
Biología Reproductiva
Bioquímica y Biología Molecular
Inglés
Instituto de Investigaciones Biológicas Clemente Estable
IIBCE en REDI
https://hdl.handle.net/20.500.12381/5518
Acceso abierto
Reconocimiento 4.0 Internacional. (CC BY)
_version_ 1875932584616132608
author Romeo-Cardeillac, Carlos
author2 Trovero, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger, Adriana
Sotelo-Silveira José
author2_role author
author
author
author
author
author
author_facet Romeo-Cardeillac, Carlos
Trovero, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger, Adriana
Sotelo-Silveira José
author_role author
bitstream.checksum.fl_str_mv fcc8b2ddb26c820405a37f9e0cae7f18
23f17ed3037eae76f02b97cad763f682
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
bitstream.url.fl_str_mv https://redi.anii.org.uy/jspui/bitstream/20.500.12381/5518/2/license.txt
https://redi.anii.org.uy/jspui/bitstream/20.500.12381/5518/1/s12864-024-10170-z.pdf
collection IIBCE en REDI
dc.creator.none.fl_str_mv Romeo-Cardeillac, Carlos
Trovero, María Fernanda
Radío, Santiago
Smircich, Pablo
Rodríguez-Casuriaga, Rosana
Geisinger, Adriana
Sotelo-Silveira José
dc.date.accessioned.none.fl_str_mv 2026-05-05T16:31:03Z
dc.date.available.none.fl_str_mv 2026-05-05T16:31:03Z
dc.date.issued.none.fl_str_mv 2024-03-20
dc.description.abstract.none.fl_txt_mv 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.sponsorship.none.fl_txt_mv Agencia Nacional de Investigación e Innovación
Comisión Sectorial Investigación Científica (CSIC, UdelaR)
dc.identifier.anii.es.fl_str_mv FCE_1_2021_1_166510
dc.identifier.doi.none.fl_str_mv 10.1186/s12864-024-10170-z
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12381/5518
dc.language.iso.none.fl_str_mv eng
dc.publisher.es.fl_str_mv BMC
dc.rights.*.fl_str_mv Acceso abierto
dc.rights.license.none.fl_str_mv Reconocimiento 4.0 Internacional. (CC BY)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.es.fl_str_mv BMC Genomics
dc.source.none.fl_str_mv reponame:IIBCE en REDI
instname:Instituto de Investigaciones Biológicas Clemente Estable
instacron:Instituto de Investigaciones Biológicas Clemente Estable
dc.subject.anii.none.fl_str_mv Ciencias Naturales y Exactas
Ciencias Biológicas
Biología Reproductiva
Bioquímica y Biología Molecular
dc.subject.es.fl_str_mv meiosis
spermatogenesis
transcriptomics
alternative splicing
lncRNAs
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.es.fl_str_mv Publicado
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description 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.
eu_rights_str_mv openAccess
format article
id IIBCE_e5dc1cc362ba51b3ab11b1ba2ca4d8e6
identifier_str_mv FCE_1_2021_1_166510
10.1186/s12864-024-10170-z
instacron_str Instituto de Investigaciones Biológicas Clemente Estable
institution Instituto de Investigaciones Biológicas Clemente Estable
instname_str Instituto de Investigaciones Biológicas Clemente Estable
language eng
network_acronym_str IIBCE
network_name_str IIBCE en REDI
oai_identifier_str oai:redi.anii.org.uy:20.500.12381/5518
publishDate 2024
reponame_str IIBCE en REDI
repository.mail.fl_str_mv vcarballo@iibce.edu.uy
repository.name.fl_str_mv IIBCE en REDI - Instituto de Investigaciones Biológicas Clemente Estable
repository_id_str 9421_3
rights_invalid_str_mv Reconocimiento 4.0 Internacional. (CC BY)
Acceso abierto
spelling Reconocimiento 4.0 Internacional. (CC BY)Acceso abiertoinfo:eu-repo/semantics/openAccess2026-05-05T16:31:03Z2026-05-05T16:31:03Z2024-03-20https://hdl.handle.net/20.500.12381/5518FCE_1_2021_1_16651010.1186/s12864-024-10170-zfrom 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.Agencia Nacional de Investigación e InnovaciónComisión Sectorial Investigación Científica (CSIC, UdelaR)engBMCBMC Genomicsreponame:IIBCE en REDIinstname:Instituto de Investigaciones Biológicas Clemente Estableinstacron:Instituto de Investigaciones Biológicas Clemente Establemeiosisspermatogenesistranscriptomicsalternative splicinglncRNAsCiencias Naturales y ExactasCiencias BiológicasBiología ReproductivaBioquímica y Biología MolecularUncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesisArtículoPublicadoinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleInstituto de Investigaciones Biológicas Clemente EstableFacultad de Ciencias (UdelaR)//Ciencias Naturales y Exactas/Ciencias Biológicas/Biología Reproductiva//Ciencias Naturales y Exactas/Ciencias Biológicas/Bioquímica y Biología MolecularRomeo-Cardeillac, CarlosTrovero, María FernandaRadío, SantiagoSmircich, PabloRodríguez-Casuriaga, RosanaGeisinger, AdrianaSotelo-Silveira JoséLICENSElicense.txtlicense.txttext/plain; charset=utf-85151https://redi.anii.org.uy/jspui/bitstream/20.500.12381/5518/2/license.txtfcc8b2ddb26c820405a37f9e0cae7f18MD52ORIGINALs12864-024-10170-z.pdfs12864-024-10170-z.pdfArtículo científicoapplication/pdf3982559https://redi.anii.org.uy/jspui/bitstream/20.500.12381/5518/1/s12864-024-10170-z.pdf23f17ed3037eae76f02b97cad763f682MD5120.500.12381/55182026-05-05 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://hdl.handle.net/20.500.12381/577Organismo científico-tecnológicohttps://www.gub.uy/ministerio-educacion-cultura/iibcehttps://redi.anii.org.uy/oai/requestvcarballo@iibce.edu.uyUruguayopendoar:9421_32026-05-05T16:31:05IIBCE en REDI - Instituto de Investigaciones Biológicas Clemente Establefalse
spellingShingle Uncovering a multitude of stage-specific splice variants and putative protein isoforms generated along mouse spermatogenesis
Romeo-Cardeillac, Carlos
meiosis
spermatogenesis
transcriptomics
alternative splicing
lncRNAs
Ciencias Naturales y Exactas
Ciencias Biológicas
Biología Reproductiva
Bioquímica y Biología Molecular
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 meiosis
spermatogenesis
transcriptomics
alternative splicing
lncRNAs
Ciencias Naturales y Exactas
Ciencias Biológicas
Biología Reproductiva
Bioquímica y Biología Molecular
url https://hdl.handle.net/20.500.12381/5518