Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast

ABSTRACT De novo genes are very important for evolutionary innovation. However, how these genes originate and spread remains largely unknown. To better understand this, we rigorously searched for de novo genes in Saccharomyces cerevisiae S288C and examined their spread and fixation in the population...

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Autores principales: Baojun Wu, Alicia Knudson
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:30c4d7b26a3a45cfba13fa4fb166ff322021-11-15T16:00:14ZTracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast10.1128/mBio.01024-182150-7511https://doaj.org/article/30c4d7b26a3a45cfba13fa4fb166ff322018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01024-18https://doaj.org/toc/2150-7511ABSTRACT De novo genes are very important for evolutionary innovation. However, how these genes originate and spread remains largely unknown. To better understand this, we rigorously searched for de novo genes in Saccharomyces cerevisiae S288C and examined their spread and fixation in the population. Here, we identified 84 de novo genes in S. cerevisiae S288C since the divergence with their sister groups. Transcriptome and ribosome profiling data revealed at least 8 (10%) and 28 (33%) de novo genes being expressed and translated only under specific conditions, respectively. DNA microarray data, based on 2-fold change, showed that 87% of the de novo genes are regulated during various biological processes, such as nutrient utilization and sporulation. Our comparative and evolutionary analyses further revealed that some factors, including single nucleotide polymorphism (SNP)/indel mutation, high GC content, and DNA shuffling, contribute to the birth of de novo genes, while domestication and natural selection drive the spread and fixation of these genes. Finally, we also provide evidence suggesting the possible parallel origin of a de novo gene between S. cerevisiae and Saccharomyces paradoxus. Together, our study provides several new insights into the origin and spread of de novo genes. IMPORTANCE Emergence of de novo genes has occurred in many lineages during evolution, but the birth, spread, and function of these genes remain unresolved. Here we have searched for de novo genes from Saccharomyces cerevisiae S288C using rigorous methods, which reduced the effects of bad annotation and genomic gaps on the identification of de novo genes. Through this analysis, we have found 84 new genes originating de novo from previously noncoding regions, 87% of which are very likely involved in various biological processes. We noticed that 10% and 33% of de novo genes were only expressed and translated under specific conditions, therefore, verification of de novo genes through transcriptome and ribosome profiling, especially from limited expression data, may underestimate the number of bona fide new genes. We further show that SNP/indel mutation, high GC content, and DNA shuffling could be involved in the birth of de novo genes, while domestication and natural selection drive the spread and fixation of these genes. Finally, we provide evidence suggesting the possible parallel origin of a new gene.Baojun WuAlicia KnudsonAmerican Society for MicrobiologyarticleDNA shufflingde novo geneGC contentparallel originspurifying selectionyeastMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic DNA shuffling
de novo gene
GC content
parallel origins
purifying selection
yeast
Microbiology
QR1-502
spellingShingle DNA shuffling
de novo gene
GC content
parallel origins
purifying selection
yeast
Microbiology
QR1-502
Baojun Wu
Alicia Knudson
Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
description ABSTRACT De novo genes are very important for evolutionary innovation. However, how these genes originate and spread remains largely unknown. To better understand this, we rigorously searched for de novo genes in Saccharomyces cerevisiae S288C and examined their spread and fixation in the population. Here, we identified 84 de novo genes in S. cerevisiae S288C since the divergence with their sister groups. Transcriptome and ribosome profiling data revealed at least 8 (10%) and 28 (33%) de novo genes being expressed and translated only under specific conditions, respectively. DNA microarray data, based on 2-fold change, showed that 87% of the de novo genes are regulated during various biological processes, such as nutrient utilization and sporulation. Our comparative and evolutionary analyses further revealed that some factors, including single nucleotide polymorphism (SNP)/indel mutation, high GC content, and DNA shuffling, contribute to the birth of de novo genes, while domestication and natural selection drive the spread and fixation of these genes. Finally, we also provide evidence suggesting the possible parallel origin of a de novo gene between S. cerevisiae and Saccharomyces paradoxus. Together, our study provides several new insights into the origin and spread of de novo genes. IMPORTANCE Emergence of de novo genes has occurred in many lineages during evolution, but the birth, spread, and function of these genes remain unresolved. Here we have searched for de novo genes from Saccharomyces cerevisiae S288C using rigorous methods, which reduced the effects of bad annotation and genomic gaps on the identification of de novo genes. Through this analysis, we have found 84 new genes originating de novo from previously noncoding regions, 87% of which are very likely involved in various biological processes. We noticed that 10% and 33% of de novo genes were only expressed and translated under specific conditions, therefore, verification of de novo genes through transcriptome and ribosome profiling, especially from limited expression data, may underestimate the number of bona fide new genes. We further show that SNP/indel mutation, high GC content, and DNA shuffling could be involved in the birth of de novo genes, while domestication and natural selection drive the spread and fixation of these genes. Finally, we provide evidence suggesting the possible parallel origin of a new gene.
format article
author Baojun Wu
Alicia Knudson
author_facet Baojun Wu
Alicia Knudson
author_sort Baojun Wu
title Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
title_short Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
title_full Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
title_fullStr Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
title_full_unstemmed Tracing the <italic toggle="yes">De Novo</italic> Origin of Protein-Coding Genes in Yeast
title_sort tracing the <italic toggle="yes">de novo</italic> origin of protein-coding genes in yeast
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/30c4d7b26a3a45cfba13fa4fb166ff32
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