Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.

Mature mammalian sperm contain a complex population of RNAs some of which might regulate spermatogenesis while others probably play a role in fertilization and early development. Due to this limited knowledge, the biological functions of sperm RNAs remain enigmatic. Here we report the first characte...

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Main Authors: Pranab J Das, Fiona McCarthy, Monika Vishnoi, Nandina Paria, Cathy Gresham, Gang Li, Priyanka Kachroo, A Kendrick Sudderth, Sheila Teague, Charles C Love, Dickson D Varner, Bhanu P Chowdhary, Terje Raudsepp
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3569414?pdf=render
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author Pranab J Das
Fiona McCarthy
Monika Vishnoi
Nandina Paria
Cathy Gresham
Gang Li
Priyanka Kachroo
A Kendrick Sudderth
Sheila Teague
Charles C Love
Dickson D Varner
Bhanu P Chowdhary
Terje Raudsepp
author_facet Pranab J Das
Fiona McCarthy
Monika Vishnoi
Nandina Paria
Cathy Gresham
Gang Li
Priyanka Kachroo
A Kendrick Sudderth
Sheila Teague
Charles C Love
Dickson D Varner
Bhanu P Chowdhary
Terje Raudsepp
author_sort Pranab J Das
collection DOAJ
description Mature mammalian sperm contain a complex population of RNAs some of which might regulate spermatogenesis while others probably play a role in fertilization and early development. Due to this limited knowledge, the biological functions of sperm RNAs remain enigmatic. Here we report the first characterization of the global transcriptome of the sperm of fertile stallions. The findings improved understanding of the biological significance of sperm RNAs which in turn will allow the discovery of sperm-based biomarkers for stallion fertility. The stallion sperm transcriptome was interrogated by analyzing sperm and testes RNA on a 21,000-element equine whole-genome oligoarray and by RNA-seq. Microarray analysis revealed 6,761 transcripts in the sperm, of which 165 were sperm-enriched, and 155 were differentially expressed between the sperm and testes. Next, 70 million raw reads were generated by RNA-seq of which 50% could be aligned with the horse reference genome. A total of 19,257 sequence tags were mapped to all horse chromosomes and the mitochondrial genome. The highest density of mapped transcripts was in gene-rich ECA11, 12 and 13, and the lowest in gene-poor ECA9 and X; 7 gene transcripts originated from ECAY. Structural annotation aligned sperm transcripts with 4,504 known horse and/or human genes, rRNAs and 82 miRNAs, whereas 13,354 sequence tags remained anonymous. The data were aligned with selected equine gene models to identify additional exons and splice variants. Gene Ontology annotations showed that sperm transcripts were associated with molecular processes (chemoattractant-activated signal transduction, ion transport) and cellular components (membranes and vesicles) related to known sperm functions at fertilization, while some messenger and micro RNAs might be critical for early development. The findings suggest that the rich repertoire of coding and non-coding RNAs in stallion sperm is not a random remnant from spermatogenesis in testes but a selectively retained and functionally coherent collection of RNAs.
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spelling doaj.art-4db3c2e40c034bf9a0813891b65116612022-12-22T01:16:32ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0182e5653510.1371/journal.pone.0056535Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.Pranab J DasFiona McCarthyMonika VishnoiNandina PariaCathy GreshamGang LiPriyanka KachrooA Kendrick SudderthSheila TeagueCharles C LoveDickson D VarnerBhanu P ChowdharyTerje RaudseppMature mammalian sperm contain a complex population of RNAs some of which might regulate spermatogenesis while others probably play a role in fertilization and early development. Due to this limited knowledge, the biological functions of sperm RNAs remain enigmatic. Here we report the first characterization of the global transcriptome of the sperm of fertile stallions. The findings improved understanding of the biological significance of sperm RNAs which in turn will allow the discovery of sperm-based biomarkers for stallion fertility. The stallion sperm transcriptome was interrogated by analyzing sperm and testes RNA on a 21,000-element equine whole-genome oligoarray and by RNA-seq. Microarray analysis revealed 6,761 transcripts in the sperm, of which 165 were sperm-enriched, and 155 were differentially expressed between the sperm and testes. Next, 70 million raw reads were generated by RNA-seq of which 50% could be aligned with the horse reference genome. A total of 19,257 sequence tags were mapped to all horse chromosomes and the mitochondrial genome. The highest density of mapped transcripts was in gene-rich ECA11, 12 and 13, and the lowest in gene-poor ECA9 and X; 7 gene transcripts originated from ECAY. Structural annotation aligned sperm transcripts with 4,504 known horse and/or human genes, rRNAs and 82 miRNAs, whereas 13,354 sequence tags remained anonymous. The data were aligned with selected equine gene models to identify additional exons and splice variants. Gene Ontology annotations showed that sperm transcripts were associated with molecular processes (chemoattractant-activated signal transduction, ion transport) and cellular components (membranes and vesicles) related to known sperm functions at fertilization, while some messenger and micro RNAs might be critical for early development. The findings suggest that the rich repertoire of coding and non-coding RNAs in stallion sperm is not a random remnant from spermatogenesis in testes but a selectively retained and functionally coherent collection of RNAs.http://europepmc.org/articles/PMC3569414?pdf=render
spellingShingle Pranab J Das
Fiona McCarthy
Monika Vishnoi
Nandina Paria
Cathy Gresham
Gang Li
Priyanka Kachroo
A Kendrick Sudderth
Sheila Teague
Charles C Love
Dickson D Varner
Bhanu P Chowdhary
Terje Raudsepp
Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
PLoS ONE
title Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
title_full Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
title_fullStr Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
title_full_unstemmed Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
title_short Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
title_sort stallion sperm transcriptome comprises functionally coherent coding and regulatory rnas as revealed by microarray analysis and rna seq
url http://europepmc.org/articles/PMC3569414?pdf=render
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