Molecular mechanism and history of non-sense to sense evolution of antifreeze glycoprotein gene in northern gadids

A fundamental question in evolutionary biology is how genetic novelty arises. De novo gene birth is a recently recognized mechanism, but the evolutionary process and function of putative de novo genes remain largely obscure. With a clear life-saving function, the diverse antifreeze proteins of polar fishes are exemplary adaptive innovations and models for investigating new gene evolution. Here, we report clear evidence and a detailed molecular mechanism for the de novo formation of the northern gadid (codfish) antifreeze glycoprotein (AFGP) gene from a minimal noncoding sequence. We constructed genomic DNA libraries for AFGP-bearing and AFGP-lacking species across the gadid phylogeny and performed fine-scale comparative analyses of theAFGPgenomic loci and homologs. We identified the noncoding founder region and a nine-nucleotide (9-nt) element therein that supplied the codons for one Thr-Ala-Ala unit from which the extant repetitive AFGP-coding sequence (cds) arose through tandem duplications. The latent signal peptide (SP)-coding exons were fortuitous noncoding DNA sequence immediately upstream of the 9-nt element, which, when spliced, supplied a typical secretory signal. Through a 1-nt frameshift mutation, these two parts formed a single read-through open reading frame (ORF). It became functionalized when a putative translocation event conferred the essentialcispromoter for transcriptional initiation. We experimentally proved that all genic components of the extant gadidAFGPoriginated from entirely nongenic DNA. The gadidAFGPevolutionary process also represents a rare example of the proto-ORF model of de novo gene birth where a fully formed ORF existed before the regulatory element to activate transcription was acquired.

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Translation of neutrally evolving peptides provides a basis for de novo gene evolution

Nature Ecology & Evolution ◽

10.1038/s41559-018-0506-6 ◽

2018 ◽

Vol 2 (5) ◽

pp. 890-896 ◽

Cited By ~ 51

Author(s):

Jorge Ruiz-Orera ◽

Pol Verdaguer-Grau ◽

José Luis Villanueva-Cañas ◽

Xavier Messeguer ◽

M. Mar Albà

Keyword(s):

De Novo ◽

Gene Evolution ◽

De Novo Gene

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The Discovery of De Novo Gene Evolution

Perspectives in Biology and Medicine ◽

10.1353/pbm.2014.0006 ◽

2014 ◽

Vol 57 (1) ◽

pp. 149-161 ◽

Cited By ~ 25

Author(s):

Diethard Tautz

Keyword(s):

De Novo ◽

Gene Evolution ◽

De Novo Gene

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Fast turnover of genome transcription across evolutionary time exposes entire non-coding DNA to de novo gene emergence

eLife ◽

10.7554/elife.09977 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 60

Author(s):

Rafik Neme ◽

Diethard Tautz

Keyword(s):

De Novo ◽

Gene Evolution ◽

Large Fraction ◽

Phylogenetic Distance ◽

Evolutionary Time ◽

High Turnover ◽

Entire Genome ◽

De Novo Gene ◽

Phylogenetic Level ◽

Transcriptome Coverage

Deep sequencing analyses have shown that a large fraction of genomes is transcribed, but the significance of this transcription is much debated. Here, we characterize the phylogenetic turnover of poly-adenylated transcripts in a comprehensive sampling of taxa of the mouse (genus Mus), spanning a phylogenetic distance of 10 Myr. Using deep RNA sequencing we find that at a given sequencing depth transcriptome coverage becomes saturated within a taxon, but keeps extending when compared between taxa, even at this very shallow phylogenetic level. Our data show a high turnover of transcriptional states between taxa and that no major transcript-free islands exist across evolutionary time. This suggests that the entire genome can be transcribed into poly-adenylated RNA when viewed at an evolutionary time scale. We conclude that any part of the non-coding genome can potentially become subject to evolutionary functionalization via de novo gene evolution within relatively short evolutionary time spans.

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The ancient Salicoid genome duplication event: A platform for reconstruction of de Novo gene evolution in Populus trichocarpa

Genome Biology and Evolution ◽

10.1093/gbe/evab198 ◽

2021 ◽

Author(s):

Timothy B Yates ◽

Kai Feng ◽

Jin Zhang ◽

Vasanth Singan ◽

Sara S Jawdy ◽

...

Keyword(s):

Genome Duplication ◽

De Novo ◽

Gene Evolution ◽

Populus Trichocarpa ◽

Duplication Event ◽

Functional Enrichment ◽

Orphan Genes ◽

Genome Duplication Event ◽

Orphan Gene ◽

De Novo Gene

Abstract Orphan genes are characteristic genomic features that have no detectable homology to genes in any other species and represent an important attribute of genome evolution as sources of novel genetic functions. Here, we identified 445 genes specific to Populus trichocarpa. Of these, we performed deeper reconstruction of 13 orphan genes to provide evidence of de novo gene evolution. Populus and its sister genera Salix are particularly well suited for the study of orphan gene evolution because of the Salicoid whole-genome duplication event (WGD) which resulted in highly syntenic sister chromosomal segments across the Salicaceae. We leveraged this genomic feature to reconstruct de novo gene evolution from inter-genera, inter-species, and intra-genomic perspectives by comparing the syntenic regions within the P. trichocarpa reference, then P. deltoides, and finally Salix purpurea. Furthermore, we demonstrated that 86.5% of the putative orphan genes had evidence of transcription. Additionally, we also utilized the Populus genome-wide association mapping panel (GWAS), a collection of 1,084 undomesticated P. trichocarpa genotypes to further determine putative regulatory networks of orphan genes using expression quantitative trait loci (eQTL) mapping. Functional enrichment of these eQTL subnetworks identified common biological themes associated with orphan genes such as response to stress and defense response. We also identify a putative cis-element for a de novo gene and leverage conserved synteny to describe evolution of a putative transcription factor binding site. Overall, 45% of orphan genes were captured in trans-eQTL networks.

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Testis single-cell RNA-seq reveals the dynamics of de novo gene transcription and germline mutational bias in Drosophila

10.1101/689687 ◽

2019 ◽

Author(s):

Evan Witt ◽

Sigi Benjamin ◽

Nicolas Svetec ◽

Li Zhao

Keyword(s):

Single Cell ◽

De Novo ◽

Gene Evolution ◽

Expression Patterns ◽

Reproductive Function ◽

Cell Types ◽

Mutational Bias ◽

Evolutionary Innovation ◽

New Genes ◽

De Novo Gene

SummaryThe testis is a peculiar tissue in many respects. It shows patterns of rapid gene evolution and provides a hotspot for the origination of genetic novelties such as de novo genes, duplications and mutations. To investigate the expression patterns of genetic novelties across cell types, we performed single-cell RNA-sequencing of adult Drosophila testis. We found that new genes were expressed in various cell types, the patterns of which may be influenced by their mode of origination. In particular, lineage-specific de novo genes are commonly expressed in early spermatocytes, while young duplicated genes are often bimodally expressed. Analysis of germline substitutions suggests that spermatogenesis is a highly reparative process, with the mutational load of germ cells decreasing as spermatogenesis progresses. By elucidating the distribution of genetic novelties across spermatogenesis, this study provides a deeper understanding of how the testis maintains its core reproductive function while being a hotbed of evolutionary innovation.

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Propagation of a De Novo Gene under Natural Selection: Antifreeze Glycoprotein Genes and Their Evolutionary History in Codfishes

Genes ◽

10.3390/genes12111777 ◽

2021 ◽

Vol 12 (11) ◽

pp. 1777

Author(s):

Xuan Zhuang ◽

C.-H. Christina Cheng

Keyword(s):

Gene Family ◽

Evolutionary History ◽

Molecular Mechanisms ◽

De Novo ◽

Sequence Divergence ◽

Coding Region ◽

Evolutionary Trajectory ◽

Antifreeze Glycoprotein ◽

De Novo Gene ◽

Rapid Sequence

The de novo birth of functional genes from non-coding DNA as an important contributor to new gene formation is increasingly supported by evidence from diverse eukaryotic lineages. However, many uncertainties remain, including how the incipient de novo genes would continue to evolve and the molecular mechanisms underlying their evolutionary trajectory. Here we address these questions by investigating evolutionary history of the de novo antifreeze glycoprotein (AFGP) gene and gene family in gadid (codfish) lineages. We examined AFGP phenotype on a phylogenetic framework encompassing a broad sampling of gadids from freezing and non-freezing habitats. In three select species representing different AFGP-bearing clades, we analyzed all AFGP gene family members and the broader scale AFGP genomic regions in detail. Codon usage analyses suggest that motif duplication produced the intragenic AFGP tripeptide coding repeats, and rapid sequence divergence post-duplication stabilized the recombination-prone long repetitive coding region. Genomic loci analyses support AFGP originated once from a single ancestral genomic origin, and shed light on how the de novo gene proliferated into a gene family. Results also show the processes of gene duplication and gene loss are distinctive in separate clades, and both genotype and phenotype are commensurate with differential local selective pressures.

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De novo gene evolution: How do we transition from non-coding to coding?

10.7287/peerj.preprints.3031 ◽

2017 ◽

Author(s):

Jorge Ruiz-Orera ◽

José Luis Villanueva-Cañas ◽

William Blevins ◽

M.Mar Albà

Keyword(s):

De Novo ◽

Gene Evolution ◽

Neutral Evolution ◽

Functional Protein ◽

Protein Coding ◽

Coding Sequences ◽

Sequence Composition ◽

Protein Coding Genes ◽

Small Proteins ◽

De Novo Gene

Recent years have witnessed the discovery of protein–coding genes which appear to have evolved de novo from previously non-coding sequences. This has changed the long-standing view that coding sequences can only evolve from other coding sequences. However, there are still many open questions regarding how new protein-coding sequences can arise from non-genic DNA. Two prerequisites for the birth of a new functional protein-coding gene are that the corresponding DNA fragment is transcribed and that it is also translated. Transcription is known to be pervasive in the genome, producing a large number of transcripts that do not correspond to conserved protein-coding genes, and which are usually annotated as long non-coding RNAs (lncRNA). Recently, sequencing of ribosome protected fragments (Ribo-Seq) has provided evidence that many of these transcripts actually translate small proteins. We have used mouse non-synonymous and synonymous variation data to estimate the strength of purifying selection acting on the translated open reading frames (ORFs). Whereas a subset of the lncRNAs are likely to actually be true protein-coding genes (and thus previously misclassified), the bulk of lncRNAs code for proteins which show variation patterns consistent with neutral evolution. We also show that the ORFs that have a more favorable, coding-like, sequence composition are more likely to be translated than other ORFs in lncRNAs. This study provides strong evidence that there is a large and ever-changing reservoir of lowly abundant proteins; some of these peptides may become useful and act as seeds for de novo gene evolution.

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Entire genome transcription across evolutionary time exposes non-coding DNA to de novo gene emergence

10.1101/017152 ◽

2015 ◽

Author(s):

Rafik Neme ◽

Diethard Tautz

Keyword(s):

De Novo ◽

Gene Evolution ◽

Sequencing Analysis ◽

Phylogenetic Distance ◽

Evolutionary Time ◽

Entire Genome ◽

De Novo Gene ◽

Mammalian Genomes ◽

Genome Transcription ◽

Deep Sequencing Analysis

Even in the best studied Mammalian genomes, less than 5% of the total genome length is annotated as exonic. However, deep sequencing analysis in humans has shown that around 40% of the genome may be covered by poly-adenylated non-coding transcripts occurring at low levels. Their functional significance is unclear, and there has been a dispute whether they should be considered as noise of the transcriptional machinery. We propose that if such transcripts show some evolutionary stability they will serve as substrates for de novo gene evolution, i.e. gene emergence out of non-coding DNA. Here, we characterize the phylogenetic turnover of low-level poly-adenylated transcripts in a comprehensive sampling of populations, sub-species and species of the genus Mus, spanning a phylogenetic distance of about 10 Myr. We find evidence for more evolutionary stable gains of transcription than losses among closely related taxa, balanced by a loss of older transcripts across the whole phylogeny. We show that adding taxa increases the genomic transcript coverage and that no major transcript-free islands exist over time. This suggests that the entire genome can be transcribed into poly-adenylated RNA when viewed at an evolutionary time scale. Thus, any part of the "non-coding" genome can become subject to evolutionary functionalization via de novo gene evolution.

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