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

Abstract

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.

Characterisation of the RNA-interference pathway as a Tool for Genetics in the Nascent Phototrophic Endosymbiosis,Paramecium bursaria

“…This observation suggests that these RNAi components are either highly expressed, and thus retention is enforced by gene dosage constraints, and/or have undergone significant neo-or sub-functionalisation driving retention of these paralogues following initial duplication59 . Our phylogenetic analysis of Dicer, RdRP and AGO-Piwi components (Datasets S1-4) supports the occurrence of at least three WGD events within the ciliate group[38][39][40] . These are hypothesised to have occurred i) after the divergence of the CONThreeP clade (Colpodea, Oligohymenophorea, Nassophorea, Prostomatea, Plagiopylea and Phyllopharyngea) 60,61 from Oxytricha trifallax (Spirotrichea) and the broader ciliates, ii) after the divergence of Paramecium from Tetrahymena thermophilia and remaining Oligohymenophorea, and iii) after the divergence of the Paramecium aurelia species complex from the remainder of the Paramecium clade (Paramecium caudatum and Paramecium bursaria).…”

“…(knock-down, rather than knock-out) is sufficient to attenuate the RNAi effect, and thereby provide an appropriate control for inferring a bona fide RNAi effect through feeding-induced siRNA-mediated gene knock-down. We have demonstrated that disruption of these essential RNAi components is effective at perturbing both background endogenous (Dcr1; Figure 3c Table 2), exceeding the 40-60% retention rate observed in paralogues of this WGD event across the Paramecium aurelia species complex 40 . This observation suggests that these RNAi components are either highly expressed, and thus retention is enforced by gene dosage constraints, and/or have undergone significant neo-or sub-functionalisation driving retention of these paralogues following initial duplication 59 .…”

“…These include orthologues of the pathway components; Dicer, Dicer-like, Piwi, Rdr, Cid and Pds1 that are present in the non-photo-endosymbiotic model system, P. tetraurelia.Our comparison across the Paramecium clade(Figure 1) reveals that many of these components likely originated from the whole genome duplication (WGD) event that occurred prior to the radiation of the Paramecium aurelia species complex that diverged separately from the P. bursaria lineage. Importantly, an unusually large number of copies of RNAicomponent encoding genes have been retained in the Paramecium clade (>80% retention for all components;Table 2), exceeding the 40-60% retention rate observed in paralogues of this WGD event across the Paramecium aurelia species complex40 . This observation suggests that these RNAi components are either highly expressed, and thus retention is enforced by gene dosage constraints, and/or have undergone significant neo-or sub-functionalisation driving retention of these paralogues following initial duplication59 .…”

Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in Arabidopsis and Maize

“…Studies have shown that redundancy between duplicate genes could lead to buffering effect against null mutations, thereby increasing the robustness of the gene regulatory network (Gu et al, 2003; Dean et al, 2008; Diss et al, 2014; Keane et al, 2014). In addition, for some duplicate genes, especially those in the same complex or involved in the same pathways, it may be important to maintain the right dosage balance (Edger and Pires, 2009; Birchler and Veitia, 2012; Wang and Chen, 2018; Gout et al, 2019). In this regard, by buffering the expression divergence established at the transcriptional level, translational regulation might fine-tune the expression level of both paralog copies, and help them better maintain the appropriate gene dosage.…”

Functional diversification of Paramecium Ku80 paralogs safeguards genome integrity during precise programmed DNA elimination

“…In addition to their different expression patterns, the two groups of P. tetraurelia KU80 paralogs issued from the intermediate WGD have diverged in their amino acid sequences: Ku80c shares 73% and 74% amino acid identity with Ku80a and Ku80b, respectively [26]. Interestingly, all P. aurelia species whose MAC genome has been sequenced [6,[30][31][32] have retained at least one ohnolog of the Ku80a type and one of the Ku80c type, whereas more distant Paramecium species, which did not undergo the last two WGDs, each encode a single version of Ku80 (S4 & S5 Figs). The conservation of Ku80c across P. aurelia species suggests that the KU80c gene has diverged not only through the acquisition of a specific transcriptional pattern during MAC development, but also through the function of its encoded protein.…”