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

Bright, Lydia J.; Goût, Jean-François; Lynch, Michael

doi:10.1091/mbc.e16-06-0361

Cited by 8 publications

(3 citation statements)

References 79 publications

(132 reference statements)

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“…This apparent lack of post-WGD phenotypic innovation is also supported by a recent study focusing on the Rab GTPase gene family which found that the recent ohnologs in this gene family did not show any sign of functional diversification (Bright, et al 2017). These observations suggest that neofunctionalization probably did not play a major role in the retention of ohnologs following the most recent genome duplication in Paramecium.…”

Section: Introductionsupporting

confidence: 58%

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

Goût

Johri

Arnaiz

et al. 2019

Preprint

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Whole-Genome Duplications (WGDs) have shaped the gene repertoire of many eukaryotic lineages.The redundancy created by WGDs typically results in a phase of massive gene loss. However, some WGD-derived paralogs are maintained over long evolutionary periods and the relative contributions of different selective pressures to their maintenance is still debated. Previous studies have revealed a history of three successive WGDs in the lineage of the ciliate Paramecium tetraurelia and two of its sister species from the P. aurelia complex. Here, we report the genome sequence and analysis of 10 additional P. aurelia species and one additional outgroup, allowing us to track post-WGD evolution in 13 species that share a common ancestral WGD. We found similar biases in gene retention compatible with dosage constraints playing a major role opposing post-WGD gene loss across all 13 species.Interestingly we found that post-WGD gene loss was slower in Paramecium than in other species having experienced genome duplication, suggesting that the selective pressures against post-WGD gene loss are especially strong in Paramecium. We also report a lack of recent segmental duplications in Paramecium, which we interpret as additional evidence for strong selective pressures against individual genes dosage changes. Finally, we hope that this exceptional dataset of 13 species sharing an ancestral WGD and two closely related outgroup species will be a useful resource for future studies and will help establish Paramecium as a major model organism in the study of post-WGD evolution.

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Section: Introductionsupporting

confidence: 58%

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

Goût

Johri

Arnaiz

et al. 2019

Preprint

Self Cite

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“…Previous studies have shown that genes that are sensitive to dosage balance and those encoding proteins with a high number of interactions are more likely to be retained after WGD events ( Freeling and Thomas 2006 ; McGrath et al 2014 ; Bright et al 2017 ). Hence, we hypothesized that genes in families with high RRs would have more “central” molecular functions ( e.g.…”

Section: Resultsmentioning

confidence: 99%

Teleost Fish-Specific Preferential Retention of Pigmentation Gene-Containing Families After Whole Genome Duplications in Vertebrates

Lorin

Brunet

Laudet

et al. 2018

G3 Genes|Genomes|Genetics

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Vertebrate pigmentation is a highly diverse trait mainly determined by neural crest cell derivatives. It has been suggested that two rounds (1R/2R) of whole-genome duplications (WGDs) at the basis of vertebrates allowed changes in gene regulation associated with neural crest evolution. Subsequently, the teleost fish lineage experienced other WGDs, including the teleost-specific Ts3R before teleost radiation and the more recent Ss4R at the basis of salmonids. As the teleost lineage harbors the highest number of pigment cell types and pigmentation diversity in vertebrates, WGDs might have contributed to the evolution and diversification of the pigmentation gene repertoire in teleosts. We have compared the impact of the basal vertebrate 1R/2R duplications with that of the teleost-specific Ts3R and salmonid-specific Ss4R WGDs on 181 gene families containing genes involved in pigmentation. We show that pigmentation genes (PGs) have been globally more frequently retained as duplicates than other genes after Ts3R and Ss4R but not after the early 1R/2R. This is also true for non-pigmentary paralogs of PGs, suggesting that the function in pigmentation is not the sole key driver of gene retention after WGDs. On the long-term, specific categories of PGs have been repeatedly preferentially retained after ancient 1R/2R and Ts3R WGDs, possibly linked to the molecular nature of their proteins (e.g., DNA binding transcriptional regulators) and their central position in protein-protein interaction networks. Taken together, our results support a major role of WGDs in the diversification of the pigmentation gene repertoire in the teleost lineage, with a possible link with the diversity of pigment cell lineages observed in these animals compared to other vertebrates.

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“…One pathway became two, and by simple iteration, many. This mechanism, the `organelle paralogy hypothesis’, found experimental support and has been elaborated upon repeatedly since the original proposal [ 2 , 9 , 17 • , 18 , 19 • , 20 , 21 ].…”

Section: How Did Complex Membrane Trafficking Evolve?mentioning

confidence: 91%

Evolutionary origins and specialisation of membrane transport

Dacks

Field

2018

Current Opinion in Cell Biology

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From unicellular protists to the largest megafauna and flora, all eukaryotes depend upon the organelles and processes of the intracellular membrane trafficking system. Well-defined machinery selectively packages and delivers material between endomembrane organelles and imports and exports material from the cell surface. This process underlies intracellular compartmentalization and facilitates myriad processes that define eukaryotic biology. Membrane trafficking is a landmark in the origins of the eukaryotic cell and recent work has begun to unravel how the revolution in cellular structure occurred.

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

Abstract: Rab GTPase family members in Paramecium have higher retention rates and more-divergent expression levels than other genes after whole-genome duplications, consistent with early steps in functional diversification. Localization analysis also uncovers functionally diversifying Rab11 genes.

Cited by 8 publications

References 79 publications

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

Teleost Fish-Specific Preferential Retention of Pigmentation Gene-Containing Families After Whole Genome Duplications in Vertebrates

Evolutionary origins and specialisation of membrane transport

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