Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra

Barrera‐Redondo, Josué; Lotharukpong, Jaruwatana Sodai; Drost, Hajk-Georg; Coelho, Susana M.

doi:10.1186/s13059-023-02895-z

Cited by 19 publications

(23 citation statements)

References 102 publications

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“…We used an evolutionary transcriptomics approach to test the developmental hourglass hypothesis for the early development of the two Fucus species. We first collected stage-specific RNAseq data ( Table S1 ) and assigned phylogenetic ages to each protein-coding gene using GenEra (Barrera-Redondo et al 2023) ( Fig. S1 ).…”

Section: Resultsmentioning

confidence: 99%

A Transcriptomic Hourglass In Brown Algae

Lotharukpong,

Zheng,

Luthringer

et al. 2024

Preprint

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Complex multicellularity has emerged independently across a few eukaryotic lineages and is often associated with the rise of elaborate, tightly coordinated developmental processes. How multicellularity and development are interconnected in evolution is a major question in biology. The hourglass model of embryonic evolution depicts how developmental processes are conserved during evolution, predicting morphological and molecular divergence in early and late embryo stages, bridged by a conserved mid-embryonic (phylotypic) period linked to the formation of the basic body plan. Initially found in animal embryos, molecular hourglass patterns have recently been proposed for land plants and fungi. However, whether the hourglass pattern is an intrinsic feature of all developmentally complex eukaryotic lineages remains elusive. Here, we tested the prevalence of a (molecular) hourglass in the brown algae, the third most developmentally complex lineage on earth that has evolved multicellularity independently from animals, fungi, and plants. By exploring the evolutionary transcriptome of brown algae with distinct morphological complexities, we uncovered an hourglass pattern during embryogenesis in developmentally complex species. Filamentous algae without a canonical embryogenesis display an evolutionary transcriptome that is most conserved in multicellular stages of the life cycle, whereas unicellular stages are more rapidly evolving. Our findings suggest that transcriptome conservation in brown algae is associated with cell differentiation stages, but not necessarily linked to embryogenesis. Together with previous work in animals, plants and fungi, we provide further evidence for the generality of a developmental hourglass pattern across complex multicellular eukaryotes.

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Section: Resultsmentioning

confidence: 99%

A Transcriptomic Hourglass In Brown Algae

Lotharukpong,

Zheng,

Luthringer

et al. 2024

Preprint

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“…Using a genomic phylostratigraphy approach (Barrera-Redondo et al 2023), we found that, overall, brittle star arm regeneration is mediated by ancient genes (i.e. metazoan or older; Figure 5A , Methods ).…”

Section: Resultsmentioning

confidence: 99%

The brittle star genome illuminates the genetic basis of animal appendage regeneration

Parey,

Ortega-Martinez,

Delroisse

et al. 2023

Preprint

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Species within nearly all extant animal lineages are capable of regenerating body parts. However, it remains unclear whether the gene expression programme controlling regeneration is evolutionarily conserved. Brittle stars are a species-rich class of echinoderms with outstanding regenerative abilities, but investigations into the genetic bases of regeneration in this group have been hindered by the limited genomic resources. Here, we report a chromosome-scale genome assembly for the brittle starAmphiura filiformis.We show that the brittle star genome is the most rearranged amongst echinoderms sequenced to date, featuring a reorganised Hox cluster reminiscent of the rearrangements observed in sea urchins. In addition, we performed an extensive profiling of gene expression during brittle star adult arm regeneration and identified sequential waves of gene expression governing wound healing, proliferation and differentiation. We conducted comparative transcriptomic analyses with other invertebrate and vertebrate models for appendage regeneration and uncovered hundreds of genes with conserved expression dynamics, particularly during the proliferative phase of regeneration. Our findings emphasise the crucial importance of echinoderms to detect long-range expression conservation between vertebrates and classical invertebrate regeneration model systems.

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“…Specifically, DENSE starts from the genome of the focal species and those of its neighboring species along with their corresponding phylogenetic tree. Then based on the phylostratigraphy calculated by GenEra (Barrera-Redondo et al, 2023), it predicts the date of emergence of all annotated coding sequences (CDSs) of the focal genome with the assumption that horizontal transfers are rare in eukaryotic species. To do so, GenEra screens each CDS against the nr database and the annotated CDSs of the neighboring genomes with DIAMONDv2 (Buchfink et al, 2021)(Figure 1A).…”

Section: Principle Of Densementioning

confidence: 99%

“…The latter correspond to genes found in a single species (i.e., orphan genes) or closely related species, a prerequisite for finding young de novo emerged genes. The detection of TRGs generally relies on phylostratigraphy that estimates the age of a gene of interest from the detection of its homologs across a phylogeny (Arendsee, Li, Singh, Seetharam, et al, 2019; Barrera-Redondo et al, 2023; Domazet-Loso et al, 2007). In practice, the idea is to screen each gene of the focal genome against a large sequence database (typically, nr or uniprot) with BLAST or an equivalent tool (Altschul et al, 1990; Buchfink et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

DE Novo emerged gene SEarch in Eukaryotes with DENSE

Roginski,

Grandchamp,

Quignot

et al. 2024

Preprint

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The discovery of de novo emerged genes, originating from previously noncoding DNA regions, challenges traditional views of species evolution. Indeed, the hypothesis of neutrally evolving sequences giving rise to functional proteins is highly unlikely. This conundrum has sparked numerous studies to quantify and characterize these genes, aiming to understand their functional roles and contributions to genome evolution. Yet, no fully automated pipeline for their identification is available. Therefore, we introduce DENSE (DE Novo emerged gene Search), an automated Nextflow pipeline based on two distinct steps: detection of Taxonomically Restricted Genes (TRGs) through phylostratigraphy, and filtering of TRGs for de novo emerged genes via genome comparisons and synteny search. DENSE is available as a user-friendly command-line tool, while the second step is accessible through a web server upon providing a list of TRGs. Highly flexible, DENSE provides various strategy and parameter combinations, enabling users to adapt to specific configurations or define their own strategy through a rational framework, facilitating protocol communication, and study interoperability. We apply DENSE to seven model organisms, exploring the impact of its strategies and parameters on de novo gene predictions. This thorough analysis across species with different evolutionary rates reveals useful metrics for users to define input datasets, identify favorable/unfavorable conditions for de novo gene detection, and control potential biases in genome annotations. Additionally, predictions made for the seven model organisms are compiled into a requestable database, that we hope will serve as a reference for de novo emerged gene lists generated with specific criteria combinations.

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Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra

Cited by 19 publications

References 102 publications

A Transcriptomic Hourglass In Brown Algae

A Transcriptomic Hourglass In Brown Algae

The brittle star genome illuminates the genetic basis of animal appendage regeneration

DE Novo emerged gene SEarch in Eukaryotes with DENSE

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