The molecular basis of monopolin recruitment to the kinetochore

Plowman, Rebecca; Singh, Namit; Tromer, Eelco C.; Payan, Angel; Duro, Eris; Spanos, Christos; Rappsilber, Juri; Snel, Berend; Kops, Geert J.P.L.; Corbett, K.D.; Marston, Adèle L.

doi:10.1007/s00412-019-00700-0

Cited by 21 publications

(28 citation statements)

References 64 publications

(137 reference statements)

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“…To study how the LECA kinetochore originated, we first needed to determine what proteins constituted it. While we reconstructed the LECA kinetochore previously (10), here we extend our analyses with Nkp1, Nkp2, and Csm1 (19) ( SI Appendix , Text ). For each protein present in human and yeast kinetochores, we asked ( i ) whether it was likely encoded in the genome of LECA, based on its distribution across the eukaryotic tree of life, and ( ii ) whether it likely operated in the LECA kinetochore, based on functional information.…”

Section: Resultsmentioning

confidence: 99%

Mosaic origin of the eukaryotic kinetochore

Tromer

Hooff

Kops

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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127

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The emergence of eukaryotes from ancient prokaryotic lineages embodied a remarkable increase in cellular complexity. While prokaryotes operate simple systems to connect DNA to the segregation machinery during cell division, eukaryotes use a highly complex protein assembly known as the kinetochore. Although conceptually similar, prokaryotic segregation systems and the eukaryotic kinetochore are not homologous. Here we investigate the origins of the kinetochore before the last eukaryotic common ancestor (LECA) using phylogenetic trees, sensitive profile-versus-profile homology detection, and structural comparisons of its protein components. We show that LECA’s kinetochore proteins share deep evolutionary histories with proteins involved in a few prokaryotic systems and a multitude of eukaryotic processes, including ubiquitination, transcription, and flagellar and vesicular transport systems. We find that gene duplications played a major role in shaping the kinetochore; more than half of LECA’s kinetochore proteins have other kinetochore proteins as closest homologs. Some of these have no detectable homology to any other eukaryotic protein, suggesting that they arose as kinetochore-specific folds before LECA. We propose that the primordial kinetochore evolved from proteins involved in various (pre)eukaryotic systems as well as evolutionarily novel folds, after which a subset duplicated to give rise to the complex kinetochore of LECA.

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Section: Resultsmentioning

confidence: 99%

Mosaic origin of the eukaryotic kinetochore

Tromer

Hooff

Kops

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

127

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“…This suggests that Spo13 recruits or maintains monopolin at kinetochores in a Cdc5-independent manner. The kinetochore recruitment of monopolin depends on its association with the core kinetochore protein, Dsn1, an interaction that is likely to be regulated by phosphorylation ( Corbett et al., 2010 , Plowman et al., 2018 , Sarkar et al., 2013 ). Spo13 also associates with, and influences, two further kinases, DDK and Hrr25, both of which are required for monopolin association with kinetochores ( Matos et al., 2008 , Petronczki et al., 2006 ).…”

Section: Discussionmentioning

confidence: 99%

Reductional Meiosis I Chromosome Segregation Is Established by Coordination of Key Meiotic Kinases

et al. 2019

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Summary Meiosis produces gametes through a specialized, two-step cell division, which is highly error prone in humans. Reductional meiosis I, where maternal and paternal chromosomes (homologs) segregate, is followed by equational meiosis II, where sister chromatids separate. Uniquely during meiosis I, sister kinetochores are monooriented and pericentromeric cohesin is protected. Here, we demonstrate that these key adaptations for reductional chromosome segregation are achieved through separable control of multiple kinases by the meiosis-I-specific budding yeast Spo13 protein. Recruitment of Polo kinase to kinetochores directs monoorientation, while independently, cohesin protection is achieved by containing the effects of cohesin kinases. Therefore, reductional chromosome segregation, the defining feature of meiosis, is established by multifaceted kinase control by a master regulator. The recent identification of Spo13 orthologs, fission yeast Moa1 and mouse MEIKIN, suggests that kinase coordination by a meiosis I regulator may be a general feature in the establishment of reductional chromosome segregation.

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“…In budding yeast whose point centromeres contain a single CENPA nucleosome, co-orientation during meiosis I depends on a monopolin complex, the core of which is the V shaped Csm1 heterodimer, that thought to confer co-orientation by cross-linking sister kinetochores (Corbett and Harrison, 2012; Rabitsch et al, 2003; Sarkar et al, 2013). Because Csm1 has little or no role in co-orientation in the fission yeast S.pombe (Gregan et al, 2008) and indeed is absent from metazoan genomes (Plowman et al, 2019), some other mechanism must confer co-orientation in eukaryotes with regional centromeres. In fission yeast, a meiosis-specific version of cohesin containing a Rec8 kleisin subunit is necessary to prevent bi-orientation during meiosis I (Watanabe and Nurse, 1999; Sakuno et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

Ogushi

Rattani

Godwin

et al. 2020

Preprint

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2 Summary Protection of peri-centromeric REC8 cohesin from separase and sister kinetochore attachment to microtubules emanating from the same spindle pole (co-orientation) ensure that sister chromatids remain associated after meiosis I. Both features are lost during meiosis II, when sister kinetochores bi-orient and lose peri-centromeric REC8 protection, resulting in sister chromatid disjunction and the production of haploid gametes. By transferring spindle-chromosome complexes (SCCs) between meiosis I and II cells, we have discovered that both sister kinetochore co-orientation and pericentromeric cohesin protection depend on the SCC and not the cytoplasm. Moreover, the catalytic activity of separase at meiosis I is necessary not only for converting kinetochores from a co-to a bi-oriented state but also for deprotection of pericentromeric cohesin and that cleavage of REC8 may be the key event. Crucially, we show that selective cleavage of REC8 in the vicinity of kinetochores is sufficient to destroy co-orientation in univalent chromosomes, albeit not in bivalents where resolution of chiasmata through cleavage of Rec8 along chromosome arms may also be required. 65the fission yeast S.pombe (Gregan et al., 2008) and indeed is absent from metazoan 66 genomes (Plowman et al., 2019), some other mechanism must confer co-orientation in 67 eukaryotes with regional centromeres. In fission yeast, a meiosis-specific version of 68 cohesin containing a Rec8 kleisin subunit is necessary to prevent bi-orientation during 69 meiosis I (Watanabe and Nurse, 1999; Sakuno et al, 2009). This suggests that cohesin 70 5 mediates co-orientation by holding sister centromeres together. Though plausible, this 71 hypothesis has never been rigorously proven. In an attempt to target specifically the 72 centromeric cohesin population for cleavage using fission yeast strains expressing a 73 CenpC-TEV fusion and Rec8 containing TEV sites, there was little or no evidence that 74 centromeric cohesin was more depleted than peri-centromeric cohesin (Yokobayashi & 75 Watanabe, 2005). 77Another important meiotic regulatory factor both in fungi and metazoa is a family of 78 proteins related to Spo13 in budding yeast (Wang et al., 1987). These include Moa1 in 79 fission yeast (Yokobayashi & Watanabe, 2005) and Meikin (Kim et al., 2015) in 80 mammals. Though not highly conserved in amino-acid sequences, all members of the 81 family are expressed exclusively during meiosis and have the property of recruiting 82 Polo-like kinases to kinetochores. Because their ablation compromises protection of 83 peri-centromeric cohesion by Shugoshin/Mei-S332 proteins (Katis et al., 2004a;84 Klapholz & Esposito, 1980; Lee et al., 2004; Shonn et al., 2002) and regulation of the 85 anaphase-promoting complex/cyclosome (APC/C) activity (Katis et al., 2004b) as well 86 as co-orientation (Galander et al., 2019; Kim et al., 2015; Matos et al., 2008; Miyazaki 87 et al., 2017), these Spo13-like proteins should be viewed as factors that regulate 88 directly or indirectly numerous...

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The molecular basis of monopolin recruitment to the kinetochore

Cited by 21 publications

References 64 publications

Mosaic origin of the eukaryotic kinetochore

Mosaic origin of the eukaryotic kinetochore

Reductional Meiosis I Chromosome Segregation Is Established by Coordination of Key Meiotic Kinases

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

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