Uncoupled evolution of the Polycomb system and deep origin of non-canonical PRC1

Potter, Bastiaan de; Raas, Maximilian W.D.; Seidl, Michael; Verrijzer, C. Peter; Snel, Berend

doi:10.1101/2023.04.04.535607

Cited by 2 publications

(2 citation statements)

References 82 publications

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“…To determine the presences and absences of eukaryotic SMC complex subunits across the eukaryotic tree of life, and to reconstruct their evolutionary histories, we used a eukaryotic dataset that we compiled previously 43 . This dataset contains the protein sequences of phylogenetically diverse eukaryotes, and model organisms.…”

Section: Methodsmentioning

confidence: 99%

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes

van Hooff,

Raas,

Tromer

et al. 2024

Preprint

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Across the tree of life, SMC complexes organize, segregate and regulate DNA. In contrast to prokaryotes, which often possess one SMC complex, eukaryotes usually have four such complexes. This expanded set is involved in managing the considerably larger nuclear genomes of eukaryotes, which are distributed across multiple chromosomes. Despite their essential functions, SMC complexes exhibit variations across model eukaryotes, suggesting an even greater variety of these complexes that remains unexplored. Here, we aimed to uncover the diversity and evolution of SMC complexes across eukaryotes, and their deeper, prokaryotic evolutionary origins. For this, we conducted in-depth comparative genomic and phylogenetic analyses of SMC complexes. We show that the last eukaryotic common ancestor (LECA) likely had fully-fledged versions of all four complexes and that the condensin II complex was later lost at least 30 times in eukaryotes. We report evidence that proteins previously designated as functional analogs in various model organisms (e.g., Sororin, Securin, Nse5 and Nse6) are in fact genuine orthologs. Finally, we traced the prokaryotic origins of these complexes and propose that a single SMC complex duplicated in an early archaeon. Altogether, we provide a comprehensive overview of eukaryotic SMC complex diversity and evolution, both addressing and generating questions about their functioning in ancestral and contemporary organisms.

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Section: Methodsmentioning

confidence: 99%

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes

van Hooff,

Raas,

Tromer

et al. 2024

Preprint

Self Cite

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“…The eukaryotic sequence database used for the evolutionary analysis consisted of 177 predicted proteomes derived from genomes or transcriptomes and spans a representative set of species across the eukaryotic tree of life. This dataset is derived from earlier work ( Potter et al, 2023 , Preprint ), with some minor adjustments detailed in Stok et al (2023) .…”

Section: Methodsmentioning

confidence: 99%

A farnesyl-dependent structural role for CENP-E in expansion of the fibrous corona

Wu,

Raas,

Alcaraz

et al. 2023

Journal of Cell Biology

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Correct chromosome segregation during cell division depends on proper connections between spindle microtubules and kinetochores. During prometaphase, kinetochores are temporarily covered with a dense protein meshwork known as the fibrous corona. Formed by oligomerization of ROD/ZW10/ZWILCH-SPINDLY (RZZ-S) complexes, the fibrous corona promotes spindle assembly, chromosome orientation, and spindle checkpoint signaling. The molecular requirements for formation of the fibrous corona are not fully understood. Here, we show that the fibrous corona depends on the mitotic kinesin CENP-E and that poorly expanded fibrous coronas after CENP-E depletion are functionally compromised. This previously unrecognized role for CENP-E does not require its motor activity but instead is driven by farnesyl modification of its C-terminal kinetochore- and microtubule-binding domain. We show that in cells, CENP-E binds Spindly and recruits RZZ-S complexes to ectopic locations in a farnesyl-dependent manner. CENP-E is recruited to kinetochores following RZZ-S, and—while not required for RZZ-S oligomerization per se—promotes subsequent fibrous corona expansion. Our comparative genomics analyses suggest that the farnesylation motif in CENP-E orthologs emerged alongside the full RZZ-S module in an ancestral lineage close to the fungi–animal split (Obazoa), revealing potential conservation of the mechanisms for fibrous corona formation. Our results show that proper spindle assembly has a potentially conserved non-motor contribution from the kinesin CENP-E through stabilization of the fibrous corona meshwork during its formation.

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Uncoupled evolution of the Polycomb system and deep origin of non-canonical PRC1

Cited by 2 publications

References 82 publications

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes

A farnesyl-dependent structural role for CENP-E in expansion of the fibrous corona

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