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Cited by 28

The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.

From de novo to ‘de nono’: The majority of novel protein coding genes identified with phylostratigraphy are old genes or recent duplicates

Casola, Claudio·2018·Genome Biology and Evolution
DOI 10.1093/gbe/evy231PMC PMC6239577

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Abstract

The evolution of novel protein-coding genes from noncoding regions of the genome is one of the most compelling pieces of evidence for genetic innovations in nature. One popular approach to identify de novo genes is phylostratigraphy, which consists of determining the approximate time of origin (age) of a gene based on its distribution along a species phylogeny. Several studies have revealed significant flaws in determining the age of genes, including de novo genes, using phylostratigraphy alone. However, the rate of false positives in de novo gene surveys, based on phylostratigraphy, remains unknown. Here, I reanalyze the findings from three studies, two of which identified tens to hundreds of rodent-specific de novo genes adopting a phylostratigraphy-centered approach. Most putative de novo genes discovered in these investigations are no longer included in recently updated mouse gene sets. Using a combination of synteny information and sequence similarity searches, I show that ∼60% of the remaining 381 putative de novo genes share homology with genes from other vertebrates, originated through gene duplication, and/or share no synteny information with nonrodent mammals. These results led to an estimated rate of ∼12 de novo genes per million years in mouse. Contrary to a previous study (Wilson BA, Foy SG, Neme R, Masel J. 2017. Young genes are highly disordered as predicted by the preadaptation hypothesis of de novo gene birth. Nat Ecol Evol. 1:0146), I found no evidence supporting the preadaptation hypothesis of de novo gene formation. Nearly half of the de novo genes confirmed in this study are within older genes, indicating that co-option of preexisting regulatory regions and a higher GC content may facilitate the origin of novel genes.

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Fig. 1. —Features distinguishing de novo and “de nono” genes. Rectangles, solid lines, and dashed lines represent genes, nongenic syntenic regions, and nonsyntenic regions, respectively. Presence of enabler substitutions (lightning bolts), absence of inparalogs and homologs in other species, conserved synteny and lack of conserved domains characterize de novo genes. Putative de novo genes that fail to conform to one or more of these criteria represent “de nono” genes. Myr, million years.
Fig. 1. —Features distinguishing de novo and “de nono” genes. Rectangles, solid lines, and dashed lines represent genes, nongenic syntenic regions, and nonsyntenic regions, respectively. Presence of enabler substitutions (lightning bolts), absence of inparalogs and homologs in other species, conserved synteny and lack of conserved domains characterize de novo genes. Putative de novo genes that fail to conform to one or more of these criteria represent “de nono” genes. Myr, million years.CC BY-NC · PubMed Central
Fig. 2. —Examples of de novo and “de nono” rodent genes visualized through the USCS Genome Browser. (a) An intergenic de novo gene with relatively low synteny conservation across several nonrodent mammals. (b) A de novo gene (blue asterisk) overlapping with the 3′UTR of an older gene. Notice that the gene symbol is the same for the two genes, which share no coding or protein similarity. (c) Summary of “de nono” genes features. (d) A “de nono” gene (Cd52, red asterisk) with conserved flanking genes in mouse (top) and human (bottom). (e) A tandem array of keratin-associated genes including three “de nono” genes (red asterisks). (f) A “de nono” gene with no synteny conservation beyond rat. Coding exons, UTRs and introns are shown as thick blue bars, thin blue bars and lines with arrows, respectively. When annotated, alternative transcripts are shown. The conservation track (green bars and single or double lines) represents the level of sequence identity between the highlighted mouse genomic region and its orthologous regions in other mammals, based on MultiZ alignments of 60 vertebrate genomes. The height of the green bars is proportional to the level of nucleotide sequence identity. The single line indicates no bases in the aligned species due to indels, whereas the double line shows regions with one or more unalignable bases. The pale yellow coloring indicates regions with Ns. The lack of any feature in the conservation track designates a region with no alignable bases and thus a complete lack of synteny conservation.
Fig. 2. —Examples of de novo and “de nono” rodent genes visualized through the USCS Genome Browser. (a) An intergenic de novo gene with relatively low synteny conservation across several nonrodent mammals. (b) A de novo gene (blue asterisk) overlapping with the 3′UTR of an older gene. Notice that the gene symbol is the same for the two genes, which share no coding or protein similarity. (c) Summary of “de nono” genes features. (d) A “de nono” gene (Cd52, red asterisk) with conserved flanking genes in mouse (top) and human (bottom). (e) A tandem array of keratin-associated genes including three “de nono” genes (red asterisks). (f) A “de nono” gene with no synteny conservation beyond rat. Coding exons, UTRs and introns are shown as thick blue bars, thin blue bars and lines with arrows, respectively. When annotated, alternative transcripts are shown. The conservation track (green bars and single or double lines) represents the level of sequence identity between the highlighted mouse genomic region and its orthologous regions in other mammals, based on MultiZ alignments of 60 vertebrate genomes. The height of the green bars is proportional to the level of nucleotide sequence identity. The single line indicates no bases in the aligned species due to indels, whereas the double line shows regions with one or more unalignable bases. The pale yellow coloring indicates regions with Ns. The lack of any feature in the conservation track designates a region with no alignable bases and thus a complete lack of synteny conservation.CC BY-NC · PubMed Central
Fig. 3. —Comparison of intrinsic structural disorder percentage (a) and GC content (b) between de novo genes and older genes. Gray boxes shows values between first and third quartile. Medians are shown as black lines. Whiskers: minimum and maximum values excluding outliers. OP, overprinting; OL, overlapping with noncoding regions of older genes; INT, intergenic.
Fig. 3. —Comparison of intrinsic structural disorder percentage (a) and GC content (b) between de novo genes and older genes. Gray boxes shows values between first and third quartile. Medians are shown as black lines. Whiskers: minimum and maximum values excluding outliers. OP, overprinting; OL, overlapping with noncoding regions of older genes; INT, intergenic.CC BY-NC · PubMed Central

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Metadata

Authors
Casola, C.
Affiliations
Department of Ecosystem Science and Management, Texas A&M University, College Station, TX
Venue
Genome Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2018-10-22
ISSN
1759-6653
DOI
10.1093/gbe/evy231
PMC
PMC6239577
Cited by
28
References
55
Language
en
Licence
creativecommons.org/licenses/by-nc/4.0/ (am)

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