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The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster

Nearly 10% of the genes in the genome of Drosophila melanogaster are in nested structures, in which one gene is completely nested within the intron of another gene (nested and including gene, respectively). Even though the coding sequences and untranslated regions of these nested/including gene pair...

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Autores principales: Lee, Yuh Chwen G., Chang, Hsiao-Han
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3814207/
https://www.ncbi.nlm.nih.gov/pubmed/24084778
http://dx.doi.org/10.1093/gbe/evt149
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author Lee, Yuh Chwen G.
Chang, Hsiao-Han
author_facet Lee, Yuh Chwen G.
Chang, Hsiao-Han
author_sort Lee, Yuh Chwen G.
collection PubMed
description Nearly 10% of the genes in the genome of Drosophila melanogaster are in nested structures, in which one gene is completely nested within the intron of another gene (nested and including gene, respectively). Even though the coding sequences and untranslated regions of these nested/including gene pairs do not overlap, their intimate structures and the possibility of shared regulatory sequences raise questions about the evolutionary forces governing the origination and subsequent functional and evolutionary impacts of these structures. In this study, we show that nested genes experience weaker evolutionary constraint, have faster rates of protein evolution, and are expressed in fewer tissues than other genes, while including genes show the opposite patterns. Surprisingly, despite completely overlapping with each other, nested and including genes are less likely to display correlated gene expression and biological function than the nearby yet nonoverlapping genes. Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene. We found that same-strand nested genes are more likely to be single-exon genes. In addition, same-strand including genes are less likely to have known lethal or sterile phenotypes than opposite-strand including genes only when the corresponding nested genes have introns. These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures.
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spelling pubmed-38142072013-10-31 The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster Lee, Yuh Chwen G. Chang, Hsiao-Han Genome Biol Evol Letter Nearly 10% of the genes in the genome of Drosophila melanogaster are in nested structures, in which one gene is completely nested within the intron of another gene (nested and including gene, respectively). Even though the coding sequences and untranslated regions of these nested/including gene pairs do not overlap, their intimate structures and the possibility of shared regulatory sequences raise questions about the evolutionary forces governing the origination and subsequent functional and evolutionary impacts of these structures. In this study, we show that nested genes experience weaker evolutionary constraint, have faster rates of protein evolution, and are expressed in fewer tissues than other genes, while including genes show the opposite patterns. Surprisingly, despite completely overlapping with each other, nested and including genes are less likely to display correlated gene expression and biological function than the nearby yet nonoverlapping genes. Interestingly, significantly fewer nested genes are transcribed from the same strand as the including gene. We found that same-strand nested genes are more likely to be single-exon genes. In addition, same-strand including genes are less likely to have known lethal or sterile phenotypes than opposite-strand including genes only when the corresponding nested genes have introns. These results support our hypothesis that selection against potential erroneous mRNA splicing when nested and including genes are on the same strand plays an important role in the evolution of nested gene structures. Oxford University Press 2013 2013-10-01 /pmc/articles/PMC3814207/ /pubmed/24084778 http://dx.doi.org/10.1093/gbe/evt149 Text en © The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Letter
Lee, Yuh Chwen G.
Chang, Hsiao-Han
The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title_full The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title_fullStr The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title_full_unstemmed The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title_short The Evolution and Functional Significance of Nested Gene Structures in Drosophila melanogaster
title_sort evolution and functional significance of nested gene structures in drosophila melanogaster
topic Letter
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3814207/
https://www.ncbi.nlm.nih.gov/pubmed/24084778
http://dx.doi.org/10.1093/gbe/evt149
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