Mixing genome annotation methods in a comparative analysis inflates the apparent number of lineage-specific genes

Weisman, Caroline M.; Murray, Andrew W.; Eddy, Sean R.

doi:10.1016/j.cub.2022.04.085

Cited by 60 publications

(61 citation statements)

References 28 publications

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“…3 To edit and visualize the genomic information we used the Apollo genome browser v.2.0.8 (Lee et al, 2009). The manual curation of candidate gene models allowed to reduce biases produced by annotation heterogeneity (Weisman et al, 2022). Also, to validate each OBP candidate, we identified OBP functional domains with Interproscan v.5.52 (Jones et al, 2014) by comparing candidate OBPs against the Pfam database v.33.1 (Mistry et al, 2021) and Conserved Domains Database (CDD) v. 3.18 (Marchler-Bauer et al, 2005).…”

Section: Identification Of Odorant-binding Protein Gene Candidates In...mentioning

confidence: 99%

Evolution of the odorant-binding protein gene family in Drosophila

et al. 2022

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Odorant-binding proteins (OBPs) are encoded by a gene family involved in the perception of olfactory signals in insects. This chemosensory gene family has been advocated as a candidate to mediate host preference and host shifts in insects, although it also participates in other physiological processes. Remarkable differences in the OBP gene repertoire have been described across insect groups, suggesting an accelerated gene turnover rate. The genus Drosophila, is a valuable resource for ecological genomics studies since it comprises groups of ecologically diverse species and there are genome data for many of them. Here, we investigate the molecular evolution of this chemosensory gene family across 19 Drosophila genomes, including the melanogaster and repleta species groups, which are mostly associated with rotting fruit and cacti, respectively. We also compared the OBP repertoire among the closely related species of the repleta group, associated with different subfamilies of Cactaceae that represent disparate chemical challenges for the flies. We found that the gene family size varies widely between species, ranging from 39 to 54 candidate OBPs. Indeed, more than 54% of these genes are organized in clusters and located on chromosomes X, 2, and 5, with a distribution conserved throughout the genus. The family sizes in the repleta group and D. virilis (virilis-repleta radiation) were smaller than in the melanogaster group. We tested alternative evolutionary models for OBP family size and turnover rates based on different ecological scenarios. We found heterogeneous gene turnover rates (GR) in comparisons involving columnar cactus specialists, prickly pear specialists, and fruit dwellers lineages, and signals of rapid molecular evolution compatible with positive selection in specific OBP genes. Taking ours and previous results together, we propose that this chemosensory gene family is involved in host adaptation and hypothesize that the adoption of the cactophilic lifestyle in the repleta group accelerated the evolution of members of the family.

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Section: Identification Of Odorant-binding Protein Gene Candidates In...mentioning

confidence: 99%

Evolution of the odorant-binding protein gene family in Drosophila

et al. 2022

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“…S2). Another issue raised for genomic phylostratigraphy is that spurious genome annotations or comparison between annotations with different levels of quality and accuracy can overestimate the proportion of recently-evolved proteins in the analysis (23,31). To address this short-coming, GenEra is able to include an additional protein-against-nucleotide search through MMseqs2 (36) with its most sensitive parameters (s = 7.5) to reconfirm gene age assignments with an annotation-free approach solely based on six-frame alignments.…”

Section: Methodsmentioning

confidence: 99%

“…While conceptually powerful, several studies have questioned the detection sensitivity of the phylostratigraphic approach (13)(14)(15)22). Gene ages may appear younger than they actually are due to gene prediction errors in the target database (23). Previous approaches have also overlooked contamination or horizontal gene transfer across lineages, which can overestimate a gene's age in a given organism (24).…”

Section: Introductionmentioning

confidence: 99%

“…Importantly, the greatest caveat of genomic phylostratigraphy is that small and fast-evolving genes are often mis-annotated as young genes due to homology detection failure (HDF), i.e, the inability of pairwise local aligners to trace back distantly-related homologs only due to neutral sequence divergence which results in spurious patterns of TRG birth (13,15). Overall, these caveats undermine the power of the original phylostratigraphic method, motivating several authors to propose key methodological improvements to obtain a more reliable estimate of gene-family founder events (9,15,23,24,28,31,32).…”

Section: Introductionmentioning

confidence: 99%

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

Barrera‐Redondo

Lotharukpong

Drost

et al. 2022

Preprint

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The emergence of new genes is an important driver of evolutionary novelty. Yet, we lack a conceptual and computational approach that accurately traces gene-family founder events and effectively associates them with trait innovation and major radiation events. Here, we present GenEra, a DIAMOND-fuelled gene-family founder inference framework that addresses previously raised limitations and biases of founder gene detection in genomic phylostratigraphy by accounting for homology detection failure (HDF). We demonstrate how GenEra can accelerate gene-family founder computations from several months to a few days for any query genome of interest. We analyzed 30 genomes to explore the emergence of new gene families during the major evolutionary transitions in plants, animals and fungi. The detection of highly conserved protein domains in these gene families indicates that neofunctionalization of preexisting protein domains is a richer source of gene-family founder events compared with de novo gene birth. We report vastly different patterns of gene-family founder events in animal and fungi before and after accounting for HDF. Only plants exhibit a consistent pattern of founder gene emergence after accounting for HDF, suggesting they are more likely to evolve novelty through the emergence of new genes compared to opisthokonts. Finally, we show that the transition to multicellularity in streptophytes, the terrestrialization of land plants and the origin of angiosperms are associated with gene-family founder bursts, as well as the evolution of bilateral symmetry in animals.

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“…Examples of genome annotation errors include gene models that may be fragmented or multiple genes incorrectly merged, genes broken by technical errors such as fragmented assemblies or sequencing errors that produce stop codons or frameshifts, or missing genes due to a lack of evidence or divergence from the training dataset. Such errors complicate analyses of orthology typically used to define evolutionary and putative functional relationships of genes within and between species, and likely confounds estimates of shared and species-specific annotations [21]. Many examples in the literature describe the cloning and validation of a gene structure in response to identifying an error in a gene model from a genomic resource; unfortunately, these updated experimentally validated models are rarely used to correct the original resource.…”

Section: Glossarymentioning

confidence: 99%

Improving helminth genome resources in the post-genomic era

Doyle

2022

Trends in Parasitology

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Mixing genome annotation methods in a comparative analysis inflates the apparent number of lineage-specific genes

Cited by 60 publications

References 28 publications

Evolution of the odorant-binding protein gene family in Drosophila

Evolution of the odorant-binding protein gene family in Drosophila

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

Improving helminth genome resources in the post-genomic era

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