Early stages of functional diversification in the Rab GTPase gene family revealed by genomic and localization studies in Paramecium species

New gene functions arise within existing gene families as a result of gene duplication and subsequent diversification. To gain insight into the steps that led to the functional diversification of paralogues, we tracked duplicate retention patterns, expression-level divergence, and subcellular markers of functional diversification in the Rab GTPase gene family in three Paramecium aurelia species. After whole-genome duplication, Rab GTPase duplicates are more highly retained than other genes in the genome but appear to be diverging more rapidly in expression levels, consistent with early steps in functional diversification. However, by localizing specific Rab proteins in Paramecium cells, we found that paralogues from the two most recent whole-genome duplications had virtually identical localization patterns, and that less closely related paralogues showed evidence of both conservation and diversification. The functionally conserved paralogues appear to target to compartments associated with both endocytic and phagocytic recycling functions, confirming evolutionary and functional links between the two pathways in a divergent eukaryotic lineage. Because the functionally diversifying paralogues are still closely related to and derived from a clade of functionally conserved Rab11 genes, we were able to pinpoint three specific amino acid residues that may be driving the change in the localization and thus the function in these proteins.

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Synteny-Guided Resolution of Gene Trees Clarifies the Functional Impact of Whole-Genome Duplications

Molecular Biology and Evolution ◽

10.1093/molbev/msaa149 ◽

2020 ◽

Vol 37 (11) ◽

pp. 3324-3337

Author(s):

Elise Parey ◽

Alexandra Louis ◽

Cédric Cabau ◽

Yann Guiguen ◽

Hugues Roest Crollius ◽

...

Keyword(s):

Gene Families ◽

Sequence Evolution ◽

Whole Genome ◽

Gene Trees ◽

Ensembl Database ◽

Whole Genome Duplications ◽

Gene Copies ◽

Genome Duplications ◽

Phenotypic Robustness ◽

New Gene

Abstract Whole-genome duplications (WGDs) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here, we present Synteny-guided CORrection of Paralogies and Orthologies (SCORPiOs), a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-My-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,394) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

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Synteny-guided resolution of gene trees clarifies the functional impact of whole genome duplications

10.1101/2020.01.30.926915 ◽

2020 ◽

Author(s):

Elise Parey ◽

Alexandra Louis ◽

Cédric Cabau ◽

Yann Guiguen ◽

Hugues Roest Crollius ◽

...

Keyword(s):

Gene Families ◽

Sequence Evolution ◽

Whole Genome ◽

Gene Trees ◽

Ensembl Database ◽

Whole Genome Duplications ◽

Gene Copies ◽

Genome Duplications ◽

Phenotypic Robustness ◽

New Gene

AbstractWhole genome duplications (WGD) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here we present SCORPiOs, a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-million-year-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,391) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

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Case Studies of Seven Gene Families with Unusual High Retention Rate Since the Vertebrate and Teleost Whole-Genome Duplications

Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts ◽

10.1007/978-3-319-61569-1_19 ◽

2017 ◽

pp. 369-396 ◽

Cited By ~ 1

Author(s):

Frédéric G. Brunet ◽

Thibault Lorin ◽

Laure Bernard ◽

Zofia Haftek-Terreau ◽

Delphine Galiana ◽

...

Keyword(s):

Case Studies ◽

Retention Rate ◽

Gene Families ◽

Whole Genome ◽

Whole Genome Duplications ◽

Genome Duplications

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Inferring putative ancient whole-genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions

GigaScience ◽

10.1093/gigascience/giaa004 ◽

2020 ◽

Vol 9 (2) ◽

Cited By ~ 8

Author(s):

Zheng Li ◽

Michael S Barker

Keyword(s):

Gene Family ◽

False Positive Rate ◽

Nuclear Gene ◽

Plant Evolution ◽

Plant Genome ◽

Total Evidence ◽

Whole Genome ◽

Green Plants ◽

Whole Genome Duplications ◽

Genome Duplications

Abstract Background Polyploidy, or whole-genome duplications (WGDs), repeatedly occurred during green plant evolution. To examine the evolutionary history of green plants in a phylogenomic framework, the 1KP project sequenced >1,000 transcriptomes across the Viridiplantae. The 1KP project provided a unique opportunity to study the distribution and occurrence of WGDs across the green plants. As an accompaniment to the capstone publication, this article provides expanded methodological details, results validation, and descriptions of newly released datasets that will aid researchers who wish to use the extended data generated by the 1KP project. Results In the 1KP capstone analyses, we used a total evidence approach that combined inferences of WGDs from Ks and phylogenomic methods to infer and place 244 putative ancient WGDs across the Viridiplantae. Here, we provide an expanded explanation of our approach by describing our methodology and walk-through examples. We also evaluated the consistency of our WGD inferences by comparing them to evidence from published syntenic analyses of plant genome assemblies. We find that our inferences are consistent with whole-genome synteny analyses and our total evidence approach may minimize the false-positive rate throughout the dataset. Conclusions We release 383,679 nuclear gene family phylogenies and 2,306 gene age distributions with Ks plots from the 1KP capstone paper. These resources will be useful for many future analyses on gene and genome evolution in green plants.

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Whole-Genome Duplications Spurred the Functional Diversification of the Globin Gene Superfamily in Vertebrates

Molecular Biology and Evolution ◽

10.1093/molbev/msr207 ◽

2011 ◽

Vol 29 (1) ◽

pp. 303-312 ◽

Cited By ~ 67

Author(s):

Federico G. Hoffmann ◽

Juan C. Opazo ◽

Jay F. Storz

Keyword(s):

Globin Gene ◽

Whole Genome ◽

Functional Diversification ◽

Whole Genome Duplications ◽

Genome Duplications

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Whole genome duplications and expansion of the vertebrate GATA transcription factor gene family

BMC Evolutionary Biology ◽

10.1186/1471-2148-9-207 ◽

2009 ◽

Vol 9 (1) ◽

pp. 207 ◽

Cited By ~ 30

Author(s):

William Q Gillis ◽

John St John ◽

Bruce Bowerman ◽

Stephan Q Schneider

Keyword(s):

Transcription Factor ◽

Gene Family ◽

Whole Genome ◽

Transcription Factor Gene ◽

Factor Gene ◽

Whole Genome Duplications ◽

Gata Transcription Factor ◽

Genome Duplications ◽

Transcription Factor Gene Family

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Evolution of Lysine-Specific Demethylase 1 and REST Corepressor Gene Families and Their Molecular Interaction

10.21203/rs.3.rs-1106901/v1 ◽

2021 ◽

Author(s):

Montserrat Olivares ◽

Gianluca Merello ◽

Daniel Verbel ◽

Marcela Gonzalez ◽

María Andrés ◽

...

Keyword(s):

Catalytic Activity ◽

Molecular Biology ◽

Gene Families ◽

Whole Genome ◽

Model Species ◽

Whole Genome Duplications ◽

Lysine Specific Demethylase ◽

Genome Duplications ◽

History Of ◽

The Common

Abstract Lysine-specific demethylase 1A (LSD1) binds to RCOR gene family of corepressors to erase transcriptionally active marks on histones. Functional diversity in these complexes depends on the type of RCOR included, which modulates the complex´s catalytic activity. We studied the duplicative history of RCOR and LSD gene families, and analyzed the evolution of their interaction. We found that RCOR genes are the product of the two rounds of whole-genome duplications that occurred early in vertebrate evolution. In contrast, the origin of the LSD genes traces back before to the divergence of animals and plants. Coimmunoprecipitation experiments using resurrected RCOR and LSD1 proteins of the jawed vertebrate ancestor, and the common hop, date the origin of LSD1-RCOR interaction to the ancestor of animals, fungi, and plants. Overall, we trace LSD1-RCOR complex evolution and propose that animal, fungi, and plant non-model species offer advantages in addressing questions about the molecular biology of this epigenetic complex.

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Inferring putative ancient whole genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions

10.1101/735076 ◽

2019 ◽

Cited By ~ 2

Author(s):

Zheng Li ◽

Michael S Barker

Keyword(s):

Gene Family ◽

Nuclear Gene ◽

Plant Evolution ◽

Plant Genome ◽

Total Evidence ◽

Whole Genome ◽

Data Set ◽

Green Plants ◽

Whole Genome Duplications ◽

Genome Duplications

AbstractPolyploidy or whole genome duplications (WGDs) repeatedly occurred during green plant evolution. To examine the evolutionary history of green plants in a phylogenomic framework, the 1KP project sequenced over 1000 transcriptomes across the Viridiplantae. The 1KP project provided a unique opportunity to study the distribution and occurrence of WGDs across the green plants. In the 1KP capstone analyses, we used a total evidence approach that combined inferences of WGDs from Ks and phylogenomic methods to infer and place ancient WGDs. Overall, 244 putative ancient WGDs were inferred across the Viridiplantae. Here, we describe these analyses and evaluate the consistency of the WGD inferences by comparing them to evidence from published syntenic analyses of plant genome assemblies. We find that our inferences are consistent with whole genome synteny analyses and our total evidence approach may minimize the false positive rate throughout the data set. Given these resources will be useful for many future analyses on gene and genome evolution in green plants, we release 383,679 nuclear gene family phylogenies and 2,306 gene age distribution (Ks) plots from the 1KP capstone paper.

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Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

10.1101/2020.07.10.177725 ◽

2020 ◽

Cited By ~ 2

Author(s):

Amber Harper ◽

Luis Baudouin Gonzalez ◽

Anna Schönauer ◽

Michael Seiter ◽

Michaela Holzem ◽

...

Keyword(s):

Genetic Material ◽

Gene Families ◽

Comparative Approach ◽

Whole Genome ◽

Developmental Gene ◽

Spider Species ◽

Transcriptomic Data ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Horseshoe Crabs

AbstractWhole genome duplications (WGD) have occurred multiple times in the evolution of animals, including in the lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic genomic events initially produce a wealth of new genetic material, which is generally followed by extensive gene loss. It appears that developmental genes such as homeobox genes, signalling pathway components and microRNAs, however, tend to be more frequently retained in duplicate following WGD (ohnologs). These not only provide the best evidence for the occurrence of WGD, but an opportunity to study its evolutionary implications. Although these genes are relatively well studied in the context of vertebrate WGD, genomic and transcriptomic data for independent comparison in other groups are scarce, with patchy sampling of only two of the five extant arachnopulmonate orders. To improve our knowledge of developmental gene repertoires, and their evolution since the arachnopulmonate WGD, we sequenced embryonic transcriptomes from two additional spider species and two whip spider species and surveyed them for three important gene families: Hox, Wnt and frizzled. We report extensive retention of ohnologs in all four species, further supporting the arachnopulmonate WGD hypothesis. Thanks to improved sampling we were able to identify patterns of likely ohnolog retention and loss within spiders, including apparent differences between major clades. The two amblypygid species have larger ohnolog repertoires of these genes than both spiders and scorpions; including the first reported duplicated Wnt1/wg, the first Wnt10 recovered in an arachnid, and broad retention of frizzled genes. These insights shed light on the evolution of the enigmatic whip spiders, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.

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