Dataset Information

De-novo emergence of SINE retroposons during the early evolution of passerine birds.

ABSTRACT: Background:Passeriformes ("perching birds" or passerines) make up more than half of all extant bird species. The genome of the zebra finch, a passerine model organism for vocal learning, was noted previously to contain thousands of short interspersed elements (SINEs), a group of retroposons that is abundant in mammalian genomes but considered largely inactive in avian genomes. Results:Here we resolve the deep phylogenetic relationships of passerines using presence/absence patterns of SINEs. The resultant retroposon-based phylogeny provides a powerful and independent corroboration of previous sequence-based analyses. Notably, SINE activity began in the common ancestor of Eupasseres (passerines excluding the New Zealand wrens Acanthisittidae) and ceased before the rapid diversification of oscine passerines (suborder Passeri - songbirds). Furthermore, we find evidence for very recent SINE activity within suboscine passerines (suborder Tyranni), following the emergence of a SINE via acquisition of a different tRNA head as we suggest through template switching. Conclusions:We propose that the early evolution of passerines was unusual among birds in that it was accompanied by de-novo emergence and activity of SINEs. Their genomic and transcriptomic impact warrants further study in the light of the massive diversification of passerines.

SUBMITTER: Suh A

PROVIDER: S-EPMC5729268 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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<i>De-novo</i> emergence of SINE retroposons during the early evolution of passerine birds.

Suh Alexander A Bachg Sandra S Donnellan Stephen S Joseph Leo L Brosius Jürgen J Kriegs Jan Ole JO Schmitz Jürgen J

Mobile DNA 20171214

<h4>Background</h4>Passeriformes ("perching birds" or passerines) make up more than half of all extant bird species. The genome of the zebra finch, a passerine model organism for vocal learning, was noted previously to contain thousands of short interspersed elements (SINEs), a group of retroposons that is abundant in mammalian genomes but considered largely inactive in avian genomes.<h4>Results</h4>Here we resolve the deep phylogenetic relationships of passerines using presence/absence patterns ...[more]

PMID: 29255493

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Project description:BackgroundNew gene emergence is so far assumed to be mostly driven by duplication and divergence of existing genes. The possibility that entirely new genes could emerge out of the non-coding genomic background was long thought to be almost negligible. With the increasing availability of fully sequenced genomes across broad scales of phylogeny, it has become possible to systematically study the origin of new genes over time and thus revisit this question.ResultsWe have used phylostratigraphy to assess trends of gene evolution across successive phylogenetic phases, using mostly the well-annotated mouse genome as a reference. We find several significant general trends and confirm them for three other vertebrate genomes (humans, zebrafish and stickleback). Younger genes are shorter, both with respect to gene length, as well as to open reading frame length. They contain also fewer exons and have fewer recognizable domains. Average exon length, on the other hand, does not change much over time. Only the most recently evolved genes have longer exons and they are often associated with active promotor regions, i.e. are part of bidirectional promotors. We have also revisited the possibility that de novo evolution of genes could occur even within existing genes, by making use of an alternative reading frame (overprinting). We find several cases among the annotated Ensembl ORFs, where the new reading frame has emerged at a higher phylostratigraphic level than the original one. We discuss some of these overprinted genes, which include also the Hoxa9 gene where an alternative reading frame covering the homeobox has emerged within the lineage leading to rodents and primates (Euarchontoglires).ConclusionsWe suggest that the overall trends of gene emergence are more compatible with a de novo evolution model for orphan genes than a general duplication-divergence model. Hence de novo evolution of genes appears to have occurred continuously throughout evolutionary time and should therefore be considered as a general mechanism for the emergence of new gene functions.

Project description:The origin of novel genes and beneficial functions is of fundamental interest in evolutionary biology. New genes can originate from different mechanisms, including horizontal gene transfer, duplication-divergence, and de novo from noncoding DNA sequences. Comparative genomics has generated strong evidence for de novo emergence of genes in various organisms, but experimental demonstration of this process has been limited to localized randomization in preexisting structural scaffolds. This bypasses the basic requirement of de novo gene emergence, i.e., lack of an ancestral gene. We constructed highly diverse plasmid libraries encoding randomly generated open reading frames and expressed them in Escherichia coli to identify short peptides that could confer a beneficial and selectable phenotype in vivo (in a living cell). Selections on antibiotic-containing agar plates resulted in the identification of three peptides that increased aminoglycoside resistance up to 48-fold. Combining genetic and functional analyses, we show that the peptides are highly hydrophobic, and by inserting into the membrane, they reduce membrane potential, decrease aminoglycoside uptake, and thereby confer high-level resistance. This study demonstrates that randomized DNA sequences can encode peptides that confer selective benefits and illustrates how expression of random sequences could spark the origination of new genes. In addition, our results also show that this question can be addressed experimentally by expression of highly diverse sequence libraries and subsequent selection for specific functions, such as resistance to toxic compounds, the ability to rescue auxotrophic/temperature-sensitive mutants, and growth on normally nonused carbon sources, allowing the exploration of many different phenotypes.IMPORTANCEDe novo gene origination from nonfunctional DNA sequences was long assumed to be implausible. However, recent studies have shown that large fractions of genomic noncoding DNA are transcribed and translated, potentially generating new genes. Experimental validation of this process so far has been limited to comparative genomics, in vitro selections, or partial randomizations. Here, we describe selection of novel peptides in vivo using fully random synthetic expression libraries. The peptides confer aminoglycoside resistance by inserting into the bacterial membrane and thereby partly reducing membrane potential and decreasing drug uptake. Our results show that beneficial peptides can be selected from random sequence pools in vivo and support the idea that expression of noncoding sequences could spark the origination of new genes.

Dataset Information

De-novo emergence of SINE retroposons during the early evolution of passerine birds.

Publications

<i>De-novo</i> emergence of SINE retroposons during the early evolution of passerine birds.

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