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Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation

Species-specific, new, or “orphan” genes account for 10%–30% of eukaryotic genomes. Although initially considered to have limited function, an increasing number of orphan genes have been shown to provide important phenotypic innovation. How new genes acquire regulatory sequences for proper temporal...

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Autores principales: Werner, Michael S., Sieriebriennikov, Bogdan, Prabh, Neel, Loschko, Tobias, Lanz, Christa, Sommer, Ralf J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6211652/
https://www.ncbi.nlm.nih.gov/pubmed/30232198
http://dx.doi.org/10.1101/gr.234872.118
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author Werner, Michael S.
Sieriebriennikov, Bogdan
Prabh, Neel
Loschko, Tobias
Lanz, Christa
Sommer, Ralf J.
author_facet Werner, Michael S.
Sieriebriennikov, Bogdan
Prabh, Neel
Loschko, Tobias
Lanz, Christa
Sommer, Ralf J.
author_sort Werner, Michael S.
collection PubMed
description Species-specific, new, or “orphan” genes account for 10%–30% of eukaryotic genomes. Although initially considered to have limited function, an increasing number of orphan genes have been shown to provide important phenotypic innovation. How new genes acquire regulatory sequences for proper temporal and spatial expression is unknown. Orphan gene regulation may rely in part on origination in open chromatin adjacent to preexisting promoters, although this has not yet been assessed by genome-wide analysis of chromatin states. Here, we combine taxon-rich nematode phylogenies with Iso-Seq, RNA-seq, ChIP-seq, and ATAC-seq to identify the gene structure and epigenetic signature of orphan genes in the satellite model nematode Pristionchus pacificus. Consistent with previous findings, we find young genes are shorter, contain fewer exons, and are on average less strongly expressed than older genes. However, the subset of orphan genes that are expressed exhibit distinct chromatin states from similarly expressed conserved genes. Orphan gene transcription is determined by a lack of repressive histone modifications, confirming long-held hypotheses that open chromatin is important for new gene formation. Yet orphan gene start sites more closely resemble enhancers defined by H3K4me1, H3K27ac, and ATAC-seq peaks, in contrast to conserved genes that exhibit traditional promoters defined by H3K4me3 and H3K27ac. Although the majority of orphan genes are located on chromosome arms that contain high recombination rates and repressive histone marks, strongly expressed orphan genes are more randomly distributed. Our results support a model of new gene origination by rare integration into open chromatin near enhancers.
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spelling pubmed-62116522018-11-13 Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation Werner, Michael S. Sieriebriennikov, Bogdan Prabh, Neel Loschko, Tobias Lanz, Christa Sommer, Ralf J. Genome Res Research Species-specific, new, or “orphan” genes account for 10%–30% of eukaryotic genomes. Although initially considered to have limited function, an increasing number of orphan genes have been shown to provide important phenotypic innovation. How new genes acquire regulatory sequences for proper temporal and spatial expression is unknown. Orphan gene regulation may rely in part on origination in open chromatin adjacent to preexisting promoters, although this has not yet been assessed by genome-wide analysis of chromatin states. Here, we combine taxon-rich nematode phylogenies with Iso-Seq, RNA-seq, ChIP-seq, and ATAC-seq to identify the gene structure and epigenetic signature of orphan genes in the satellite model nematode Pristionchus pacificus. Consistent with previous findings, we find young genes are shorter, contain fewer exons, and are on average less strongly expressed than older genes. However, the subset of orphan genes that are expressed exhibit distinct chromatin states from similarly expressed conserved genes. Orphan gene transcription is determined by a lack of repressive histone modifications, confirming long-held hypotheses that open chromatin is important for new gene formation. Yet orphan gene start sites more closely resemble enhancers defined by H3K4me1, H3K27ac, and ATAC-seq peaks, in contrast to conserved genes that exhibit traditional promoters defined by H3K4me3 and H3K27ac. Although the majority of orphan genes are located on chromosome arms that contain high recombination rates and repressive histone marks, strongly expressed orphan genes are more randomly distributed. Our results support a model of new gene origination by rare integration into open chromatin near enhancers. Cold Spring Harbor Laboratory Press 2018-11 /pmc/articles/PMC6211652/ /pubmed/30232198 http://dx.doi.org/10.1101/gr.234872.118 Text en © 2018 Werner et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Werner, Michael S.
Sieriebriennikov, Bogdan
Prabh, Neel
Loschko, Tobias
Lanz, Christa
Sommer, Ralf J.
Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title_full Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title_fullStr Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title_full_unstemmed Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title_short Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
title_sort young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6211652/
https://www.ncbi.nlm.nih.gov/pubmed/30232198
http://dx.doi.org/10.1101/gr.234872.118
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