scholarly journals Yeast de novo genes preferentially emerge from divergently transcribed, GC-rich intergenic regions

2017 ◽  
Author(s):  
Nikolaos Vakirlis N ◽  
Alex S Hebert ◽  
Dana A Opulente ◽  
Guillaume Achaz ◽  
Chris Todd Hittinger ◽  
...  
Keyword(s):  
Evolutionary Biology ◽  
De Novo ◽  
Genetic Network ◽  
Protein Coding ◽  
New Genes ◽  
Intergenic Sequences ◽  
Protein Functions ◽  
Intergenic Regions ◽  
Recombination Hot Spots ◽  
Remote Homologs

AbstractNew genes, with novel protein functions, can evolve “from scratch” out of intergenic sequences. These de novo genes can integrate the cell’s genetic network and drive important phenotypic innovations. Therefore, identifying de novo genes and understanding how the transition from noncoding to coding occurs are key problems in evolutionary biology. However, identifying de novo genes is a difficult task, hampered by the presence of remote homologs, fast evolving sequences and erroneously annotated protein coding genes. To overcome these limitations, we developed a procedure that handles the usual pitfalls in de novo gene identification and predicted the emergence of 703 de novo genes in 15 yeast species from two genera whose phylogeny spans at least 100 million years of evolution. We established that de novo gene origination is a widespread phenomenon in yeasts, only a few being ultimately maintained by selection. We validated 82 candidates, by providing new translation evidence for 25 of them through mass spectrometry experiments. We also unambiguously identified the mutations that enabled the transition from non-coding to coding for 30 Saccharomyces de novo genes. We found that de novo genes preferentially emerge next to divergent promoters in GC-rich intergenic regions where the probability of finding a fortuitous and transcribed ORF is the highest. We found a more than 3-fold enrichment of de novo genes at recombination hot spots, which are GC-rich and nucleosome-free regions, suggesting that meiotic recombination would be a major driving force of de novo gene emergence in yeasts.

scholarly journals De novoemergence of adaptive membrane proteins from thymine-rich intergenic sequences

2019 ◽  
Author(s):  
Nikolaos Vakirlis ◽  
Omer Acar ◽  
Brian Hsu ◽  
Nelson Castilho Coelho ◽  
S. Branden Van Oss ◽  
...  
Keyword(s):  
De Novo ◽  
Transmembrane Proteins ◽  
Protein Coding ◽  
Coding Sequences ◽  
Beneficial Effects ◽  
Protein Coding Genes ◽  
Evolutionary Innovation ◽  
Intergenic Sequences ◽  
Intergenic Regions ◽  
Novel Protein

SummaryRecent evidence demonstrates that novel protein-coding genes can arisede novofrom intergenic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of intergenic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Do intergenic translation events yield polypeptides with useful biochemical capacities? The answer to this question remains controversial. Here, we systematically characterized howde novoemerging coding sequences impact fitness. In budding yeast, overexpression of these sequences was enriched in beneficial effects, while their disruption was generally inconsequential. We found that beneficial emerging sequences have a strong tendency to encode putative transmembrane proteins, which appears to stem from a cryptic propensity for transmembrane signals throughout thymine-rich intergenic regions of the genome. These findings suggest that novel genes with useful biochemical capacities, such as transmembrane domains, tend to evolvede novowithin intergenic loci that already harbored a blueprint for these capacities.

scholarly journals Studying the dawn of de novo gene emergence in mice reveals fast integration of new genes into functional networks

2019 ◽  
Author(s):  
Chen Xie ◽  
Cemalettin Bekpen ◽  
Sven Künzel ◽  
Maryam Keshavarz ◽  
Rebecca Krebs-Wheaton ◽  
...  
Keyword(s):  
De Novo ◽  
Expression Patterns ◽  
Transcriptional Networks ◽  
Protein Coding ◽  
Protein Coding Genes ◽  
New Genes ◽  
De Novo Gene ◽  
Intergenic Sequences ◽  
Genomic Analyses ◽  
New Protein

AbstractThe de novo emergence of new transcripts has been well documented through genomic analyses. However, a functional analysis, especially of very young protein-coding genes, is still largely lacking. Here we focus on three loci that have evolved from previously intergenic sequences in the house mouse (Mus musculus) and are not present in its closest relatives. We have obtained knockouts and analyzed their phenotypes, including a deep transcriptomic analysis, based on a dedicated power analysis. We show that the transcriptional networks are significantly disturbed in the knockouts and that all three genes have effects on phenotypes that are related to their expression patterns. This includes behavioral effects, skeletal differences and the regulation of the reproduction cycle in females. Substitution analysis suggests that all three genes have directly obtained an activity, without new adaptive substitutions. Our findings support the hypothesis that de novo genes can quickly adopt functions without extensive adaptation.Impact statementNew protein-coding genes emerging out of non-coding sequences can become directly functional without signatures of adaptive protein changes

scholarly journals Diversity and evolution of the emerging Pandoraviridae family

2017 ◽  
Author(s):  
Matthieu Legendre ◽  
Elisabeth Fabre ◽  
Olivier Poirot ◽  
Sandra Jeudy ◽  
Audrey Lartigue ◽  
...  
Keyword(s):  
Comparative Genomics ◽  
De Novo ◽  
Gene Duplications ◽  
Statistical Features ◽  
Strong Component ◽  
Protein Coding ◽  
Protein Coding Genes ◽  
Intergenic Regions ◽  
Comparative Genomics Analysis ◽  
Horizontal Transfers

AbstractWith DNA genomes up to 2.5 Mb packed in particles of bacterium-like shape and dimension, the first two Acanthamoeba-infectingPandoravirusesremained the most spectacular viruses since their description in 2013. Our isolation of three new strains from distant locations and environments allowed us to perform the first comparative genomics analysis of the emerging worldwide-distributed Pandoraviridae family. Thorough annotation of the genomes combining transcriptomic, proteomic, and bioinformatic analyses, led to the discovery of many non-coding transcripts while significantly reducing the former set of predicted protein-coding genes. We found that the Pandoraviridae exhibit an open pan genome, the enormous size of which is not adequately explained by gene duplications or horizontal transfers. As most of the strain specific genes have no extant homolog and exhibit statistical features comparable to intergenic regions, we suggests thatde novogene creation is a strong component in the evolution of the giant Pandoravirus genomes.

scholarly journals A de novo evolved gene in the house mouse regulates female pregnancy cycles

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Chen Xie ◽  
Cemalettin Bekpen ◽  
Sven Künzel ◽  
Maryam Keshavarz ◽  
Rebecca Krebs-Wheaton ◽  
...  
Keyword(s):  
House Mouse ◽  
De Novo ◽  
Specific Protein ◽  
Ribosome Profiling ◽  
Mass Spectrometry Data ◽  
Preimplantation Embryos ◽  
Protein Coding ◽  
Reading Frame ◽  
Protein Coding Genes ◽  
New Genes

The de novo emergence of new genes has been well documented through genomic analyses. However, a functional analysis, especially of very young protein-coding genes, is still largely lacking. Here, we identify a set of house mouse-specific protein-coding genes and assess their translation by ribosome profiling and mass spectrometry data. We functionally analyze one of them, Gm13030, which is specifically expressed in females in the oviduct. The interruption of the reading frame affects the transcriptional network in the oviducts at a specific stage of the estrous cycle. This includes the upregulation of Dcpp genes, which are known to stimulate the growth of preimplantation embryos. As a consequence, knockout females have their second litters after shorter times and have a higher infanticide rate. Given that Gm13030 shows no signs of positive selection, our findings support the hypothesis that a de novo evolved gene can directly adopt a function without much sequence adaptation.

scholarly journals New Genes Born-In or Invading Vertebrate Genomes

2021 ◽  
Vol 9 ◽  
Author(s):  
Carlos Herrera-Úbeda ◽  
Jordi Garcia-Fernàndez
Keyword(s):  
Immune System ◽  
Horizontal Gene Transfer ◽  
Gene Networks ◽  
De Novo ◽  
Fundamental Question ◽  
High Tolerance ◽  
Virus Infections ◽  
Vertebrate Lineage ◽  
Protein Coding ◽  
New Genes

Which is the origin of genes is a fundamental question in Biology, indeed a question older than the discovery of genes itself. For more than a century, it was uneven to think in origins other than duplication and divergence from a previous gene. In recent years, however, the intersection of genetics, embryonic development, and bioinformatics, has brought to light that de novo generation from non-genic DNA, horizontal gene transfer and, noticeably, virus and transposon invasions, have shaped current genomes, by integrating those newcomers into old gene networks, helping to shape morphological and physiological innovations. We here summarized some of the recent research in the field, mostly in the vertebrate lineage with a focus on protein-coding novelties, showing that the placenta, the adaptative immune system, or the highly developed neocortex, among other innovations, are linked to de novo gene creation or domestication of virus and transposons. We provocatively suggest that the high tolerance to virus infections by bats may also be related to previous virus and transposon invasions in the bat lineage.

scholarly journals Pandoravirus celtis illustrates the microevolution processes at work in the giant Pandoraviridae genomes

2018 ◽  
Author(s):  
Matthieu Legendre ◽  
Jean-Marie Alempic ◽  
Nadège Philippe ◽  
Audrey Lartigue ◽  
Sandra Jeudy ◽  
...  
Keyword(s):  
De Novo ◽  
Gene Repertoire ◽  
Protein Coding ◽  
Genomic Changes ◽  
Coding Regions ◽  
Protein Coding Genes ◽  
Intergenic Regions ◽  
Mere Existence ◽  
Increasing Functions ◽  
Similar Gene

AbstractWith genomes of up to 2.7 Mb propagated in µm-long oblong particles and initially predicted to encode more than 2000 proteins, members of the Pandoraviridae family display the most extreme features of the known viral world. The mere existence of such giant viruses raises fundamental questions about their origin and the processes governing their evolution. A previous analysis of six newly available isolates, independently confirmed by a study including 3 others, established that the Pandoraviridae pan-genome is open, meaning that each new strain exhibits protein-coding genes not previously identified in other family members. With an average increment of about 60 proteins, the gene repertoire shows no sign of reaching a limit and remains largely coding for proteins without recognizable homologs in other viruses or cells (ORFans). To explain these results, we proposed that most new protein-coding genes were created de novo, from pre-existing non-coding regions of the G+C rich pandoravirus genomes. The comparison of the gene content of a new isolate, P. celtis, closely related (96% identical genome) to the previously described P. quercus is now used to test this hypothesis by studying genomic changes in a microevolution range. Our results confirm that the differences between these two similar gene contents mostly consist of protein-coding genes without known homologs (ORFans), with statistical signatures close to that of intergenic regions. These newborn proteins are under slight negative selection, perhaps to maintain stable folds and prevent protein aggregation pending the eventual emergence of fitness-increasing functions. Our study also unraveled several insertion events mediated by a transposase of the hAT family, 3 copies of which are found in P. celtis and are presumably active. Members of the Pandoraviridae are presently the first viruses known to encode this type of transposase.

scholarly journals De novo emergence of adaptive membrane proteins from thymine-rich genomic sequences

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Nikolaos Vakirlis ◽  
Omer Acar ◽  
Brian Hsu ◽  
Nelson Castilho Coelho ◽  
S. Branden Van Oss ◽  
...  
Keyword(s):  
Natural Selection ◽  
De Novo ◽  
Natural Populations ◽  
Evolutionary Model ◽  
Transmembrane Domains ◽  
Protein Coding ◽  
Fitness Effects ◽  
Evolutionary Innovation ◽  
Intergenic Regions ◽  
Novel Protein

AbstractRecent evidence demonstrates that novel protein-coding genes can arise de novo from non-genic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of non-genic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Here, we systematically characterize how these de novo emerging coding sequences impact fitness in budding yeast. Disruption of emerging sequences is generally inconsequential for fitness in the laboratory and in natural populations. Overexpression of emerging sequences, however, is enriched in adaptive fitness effects compared to overexpression of established genes. We find that adaptive emerging sequences tend to encode putative transmembrane domains, and that thymine-rich intergenic regions harbor a widespread potential to produce transmembrane domains. These findings, together with in-depth examination of the de novo emerging YBR196C-A locus, suggest a novel evolutionary model whereby adaptive transmembrane polypeptides emerge de novo from thymine-rich non-genic regions and subsequently accumulate changes molded by natural selection.

scholarly journals Genome Sequence and Architecture of the Tobacco Downy Mildew Pathogen Peronospora tabacina

2015 ◽  
Vol 28 (11) ◽  
pp. 1198-1215 ◽  
Author(s):  
Lida Derevnina ◽  
Sebastian Chin-Wo-Reyes ◽  
Frank Martin ◽  
Kelsey Wood ◽  
Lutz Froenicke ◽  
...  
Keyword(s):  
Downy Mildew ◽  
De Novo ◽  
Nuclear Genome ◽  
Peronospora Tabacina ◽  
Protein Coding ◽  
Rxlr Effectors ◽  
Intergenic Regions ◽  
High Level ◽  
Genomic Regions ◽  
Hyaloperonospora Arabidopsidis

Peronospora tabacina is an obligate biotrophic oomycete that causes blue mold or downy mildew on tobacco (Nicotiana tabacum). It is an economically important disease occurring frequently in tobacco-growing regions worldwide. We sequenced and characterized the genomes of two P. tabacina isolates and mined them for pathogenicity-related proteins and effector-encoding genes. De novo assembly of the genomes using Illumina reads resulted in 4,016 (63.1 Mb, N50 = 79 kb) and 3,245 (55.3 Mb, N50 = 61 kb) scaffolds for isolates 968-J2 and 968-S26, respectively, with an estimated genome size of 68 Mb. The mitochondrial genome has a similar size (approximately 43 kb) and structure to those of other oomycetes, plus several minor unique features. Repetitive elements, primarily retrotransposons, make up approximately 24% of the nuclear genome. Approximately 18,000 protein-coding gene models were predicted. Mining the secretome revealed approximately 120 candidate RxLR, six CRN (candidate effectors that elicit crinkling and necrosis), and 61 WY domain–containing proteins. Candidate RxLR effectors were shown to be predominantly undergoing diversifying selection, with approximately 57% located in variable gene-sparse regions of the genome. Aligning the P. tabacina genome to Hyaloperonospora arabidopsidis and Phytophthora spp. revealed a high level of synteny. Blocks of synteny show gene inversions and instances of expansion in intergenic regions. Extensive rearrangements of the gene-rich genomic regions do not appear to have occurred during the evolution of these highly variable pathogens. These assemblies provide the basis for studies of virulence in this and other downy mildew pathogens.

scholarly journals New genes and functional innovation in mammals

2016 ◽  
Author(s):  
José Luis Villanueva-Cañas ◽  
Jorge Ruiz-Orera ◽  
M.Isabel Agea ◽  
Maria Gallo ◽  
David Andreu ◽  
...  
Keyword(s):  
De Novo ◽  
Gene Families ◽  
Specific Gene ◽  
Protein Coding ◽  
Evolutionary Innovation ◽  
New Genes ◽  
Recent Origin ◽  
Mammalian Genes ◽  
Genomic Regions ◽  
New Protein

ABSTRACTThe birth of genes that encode new protein sequences is a major source of evolutionary innovation. However, we still understand relatively little about how these genes come into being and which functions they are selected for. To address these questions we have obtained a large collection of mammalian-specific gene families that lack homologues in other eukaryotic groups. We have combined gene annotations and de novo transcript assemblies from 30 different mamalian species, obtaining about 6,000 gene families. In general, the proteins in mammalian-specific gene families tend to be short and depleted in aromatic and negatively charged residues. Proteins which arose early in mammalian evolution include milk and skin polypeptides, immune response components, and proteins involved in reproduction. In contrast, the functions of proteins which have a more recent origin remain largely unknown, despite the fact that these proteins also have extensive proteomics support. We identify several previously described cases of genes originated de novo from non-coding genomic regions, supporting the idea that this mechanism frequently underlies the evolution of new protein-coding genes in mammals. Finally, we show that most young mammalian genes are preferentially expressed in testis, suggesting that sexual selection plays an important role in the emergence of new functional genes.

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