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

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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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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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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Expansion of banana (Musa acuminata) gene families involved in ethylene biosynthesis and signalling after lineage-specific whole-genome duplications

New Phytologist ◽

10.1111/nph.12710 ◽

2014 ◽

Vol 202 (3) ◽

pp. 986-1000 ◽

Cited By ~ 21

Author(s):

Cyril Jourda ◽

Céline Cardi ◽

Didier Mbéguié-A-Mbéguié ◽

Stéphanie Bocs ◽

Olivier Garsmeur ◽

...

Keyword(s):

Gene Families ◽

Ethylene Biosynthesis ◽

Musa Acuminata ◽

Whole Genome ◽

Whole Genome Duplications ◽

Genome Duplications

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

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab299 ◽

2021 ◽

Author(s):

Amber Harper ◽

Luis Baudouin Gonzalez ◽

Anna Schönauer ◽

Ralf Janssen ◽

Michael Seiter ◽

...

Keyword(s):

Whole Genome Duplication ◽

Genome Duplication ◽

Genetic Material ◽

Gene Families ◽

Comparative Approach ◽

Whole Genome ◽

Animal Evolution ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Horseshoe Crabs

Abstract Whole genome duplications have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss. It appears, however, that developmental genes such as homeobox genes, signalling pathway components and microRNAs are frequently retained as duplicates (so called ohnologs) following whole-genome duplication. These not only provide the best evidence for whole-genome duplication, but an opportunity to study its evolutionary consequences. Although these genes are well studied in the context of vertebrate whole-genome duplication, similar comparisons across the extant arachnopulmonate orders are patchy. We sequenced embryonic transcriptomes from two spider species and two amblypygid species and surveyed three important gene families, Hox, Wnt and frizzled, across these and twelve existing transcriptomic and genomic resources for chelicerates. We report extensive retention of putative ohnologs, further supporting the ancestral arachnopulmonate whole-genome duplication. We also found evidence of consistent evolutionary trajectories in Hox and Wnt gene repertoires across three of the six arachnopulmonate orders, with inter-order variation in the retention of specific paralogs. We identified variation between major clades in spiders and are better able to reconstruct the chronology of gene duplications and losses in spiders, amblypygids, and scorpions. These insights shed light on the evolution of the developmental toolkit in arachnopulmonates, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.

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

Molecular Biology of the Cell ◽

10.1091/mbc.e16-06-0361 ◽

2017 ◽

Vol 28 (8) ◽

pp. 1101-1110 ◽

Cited By ~ 4

Author(s):

Lydia J. Bright ◽

Jean-Francois Gout ◽

Michael Lynch

Keyword(s):

Gene Family ◽

Gene Families ◽

Rab Gtpase ◽

Rab Proteins ◽

Whole Genome ◽

Amino Acid Residues ◽

Functional Diversification ◽

Whole Genome Duplications ◽

Genome Duplications ◽

New Gene

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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On the Expansion of “Dangerous” Gene Repertoires by Whole-Genome Duplications in Early Vertebrates

Cell Reports ◽

10.1016/j.celrep.2012.09.034 ◽

2012 ◽

Vol 2 (5) ◽

pp. 1387-1398 ◽

Cited By ~ 34

Author(s):

Param Priya Singh ◽

Séverine Affeldt ◽

Ilaria Cascone ◽

Rasim Selimoglu ◽

Jacques Camonis ◽

...

Keyword(s):

Whole Genome ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Early Vertebrates

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Significance of whole-genome duplications on the emergence of evolutionary novelties

Briefings in Functional Genomics ◽

10.1093/bfgp/ely007 ◽

2018 ◽

Vol 17 (5) ◽

pp. 329-338 ◽

Cited By ~ 21

Author(s):

Yuuta Moriyama ◽

Kazuko Koshiba-Takeuchi

Keyword(s):

Whole Genome ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Evolutionary Novelties

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Legume Cytosolic and Plastid Acetyl-Coenzyme—A Carboxylase Genes Differ by Evolutionary Patterns and Selection Pressure Schemes Acting before and after Whole-Genome Duplications

Genes ◽

10.3390/genes9110563 ◽

2018 ◽

Vol 9 (11) ◽

pp. 563 ◽

Cited By ~ 6

Author(s):

Anna Szczepaniak ◽

Michał Książkiewicz ◽

Jan Podkowiński ◽

Katarzyna Czyż ◽

Marek Figlerowicz ◽

...

Keyword(s):

Selection Pressure ◽

Coenzyme A ◽

Phylogenetic Inference ◽

Whole Genome ◽

Evolutionary Patterns ◽

Acetyl Coenzyme A ◽

Acetyl Coenzyme ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Acetyl Coenzyme A Carboxylase

Acetyl-coenzyme A carboxylase (ACCase, E.C.6.4.1.2) catalyzes acetyl-coenzyme A carboxylation to malonyl coenzyme A. Plants possess two distinct ACCases differing by cellular compartment and function. Plastid ACCase contributes to de novo fatty acid synthesis, whereas cytosolic enzyme to the synthesis of very long chain fatty acids, phytoalexins, flavonoids, and anthocyanins. The narrow leafed lupin (Lupinus angustifolius L.) represents legumes, a plant family which evolved by whole-genome duplications (WGDs). The study aimed on the contribution of these WGDs to the multiplication of ACCase genes and their further evolutionary patterns. The molecular approach involved bacterial artificial chromosome (BAC) library screening, fluorescent in situ hybridization, linkage mapping, and BAC sequencing. In silico analysis encompassed sequence annotation, comparative mapping, selection pressure calculation, phylogenetic inference, and gene expression profiling. Among sequenced legumes, the highest number of ACCase genes was identified in lupin and soybean. The most abundant plastid ACCase subunit genes were accB. ACCase genes in legumes evolved by WGDs, evidenced by shared synteny and Bayesian phylogenetic inference. Transcriptional activity of almost all copies was confirmed. Gene duplicates were conserved by strong purifying selection, however, positive selection occurred in Arachis (accB2) and Lupinus (accC) lineages, putatively predating the WGD event(s). Early duplicated accA and accB genes underwent transcriptional sub-functionalization.

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