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Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster

Highly precise, yet flexible and responsive coordination of expression across groups of genes underpins the integrity of many vital functions. However, our understanding of gene regulatory networks (GRNs) is often hampered by the lack of experimentally tractable systems, by significant computational...

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Autores principales: Mohorianu, Irina, Fowler, Emily K., Dalmay, Tamas, Chapman, Tracey
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170815/
https://www.ncbi.nlm.nih.gov/pubmed/30257913
http://dx.doi.org/10.1098/rspb.2018.1681
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author Mohorianu, Irina
Fowler, Emily K.
Dalmay, Tamas
Chapman, Tracey
author_facet Mohorianu, Irina
Fowler, Emily K.
Dalmay, Tamas
Chapman, Tracey
author_sort Mohorianu, Irina
collection PubMed
description Highly precise, yet flexible and responsive coordination of expression across groups of genes underpins the integrity of many vital functions. However, our understanding of gene regulatory networks (GRNs) is often hampered by the lack of experimentally tractable systems, by significant computational challenges derived from the large number of genes involved or from difficulties in the accurate identification and characterization of gene interactions. Here we used a tractable experimental system in which to study GRNs: the genes encoding the seminal fluid proteins that are transferred along with sperm (the ‘transferome’) in Drosophila melanogaster fruit flies. The products of transferome genes are core determinants of reproductive success and, to date, only transcription factors have been implicated in the modulation of their expression. Hence, as yet, we know nothing about the post-transcriptional mechanisms underlying the tight, responsive and precise regulation of this important gene set. We investigated this omission in the current study. We first used bioinformatics to identify potential regulatory motifs that linked the transferome genes in a putative interaction network. This predicted the presence of putative microRNA (miRNA) ‘hubs’. We then tested this prediction, that post-transcriptional regulation is important for the control of transferome genes, by knocking down miRNA expression in adult males. This abolished the ability of males to respond adaptively to the threat of sexual competition, indicating a regulatory role for miRNAs in the regulation of transferome function. Further bioinformatics analysis then identified candidate miRNAs as putative regulatory hubs and evidence for variation in the strength of miRNA regulation across the transferome gene set. The results revealed regulatory mechanisms that can underpin robust, precise and flexible regulation of multiple fitness-related genes. They also help to explain how males can adaptively modulate ejaculate composition.
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spelling pubmed-61708152018-10-21 Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster Mohorianu, Irina Fowler, Emily K. Dalmay, Tamas Chapman, Tracey Proc Biol Sci Evolution Highly precise, yet flexible and responsive coordination of expression across groups of genes underpins the integrity of many vital functions. However, our understanding of gene regulatory networks (GRNs) is often hampered by the lack of experimentally tractable systems, by significant computational challenges derived from the large number of genes involved or from difficulties in the accurate identification and characterization of gene interactions. Here we used a tractable experimental system in which to study GRNs: the genes encoding the seminal fluid proteins that are transferred along with sperm (the ‘transferome’) in Drosophila melanogaster fruit flies. The products of transferome genes are core determinants of reproductive success and, to date, only transcription factors have been implicated in the modulation of their expression. Hence, as yet, we know nothing about the post-transcriptional mechanisms underlying the tight, responsive and precise regulation of this important gene set. We investigated this omission in the current study. We first used bioinformatics to identify potential regulatory motifs that linked the transferome genes in a putative interaction network. This predicted the presence of putative microRNA (miRNA) ‘hubs’. We then tested this prediction, that post-transcriptional regulation is important for the control of transferome genes, by knocking down miRNA expression in adult males. This abolished the ability of males to respond adaptively to the threat of sexual competition, indicating a regulatory role for miRNAs in the regulation of transferome function. Further bioinformatics analysis then identified candidate miRNAs as putative regulatory hubs and evidence for variation in the strength of miRNA regulation across the transferome gene set. The results revealed regulatory mechanisms that can underpin robust, precise and flexible regulation of multiple fitness-related genes. They also help to explain how males can adaptively modulate ejaculate composition. The Royal Society 2018-09-26 2018-09-26 /pmc/articles/PMC6170815/ /pubmed/30257913 http://dx.doi.org/10.1098/rspb.2018.1681 Text en © 2018 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Evolution
Mohorianu, Irina
Fowler, Emily K.
Dalmay, Tamas
Chapman, Tracey
Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title_full Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title_fullStr Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title_full_unstemmed Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title_short Control of seminal fluid protein expression via regulatory hubs in Drosophila melanogaster
title_sort control of seminal fluid protein expression via regulatory hubs in drosophila melanogaster
topic Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170815/
https://www.ncbi.nlm.nih.gov/pubmed/30257913
http://dx.doi.org/10.1098/rspb.2018.1681
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