Inferring the Evolutionary History of Your Favorite Protein: A Guide for Molecular Biologists

Hooff, Jolien J. E. van; Tromer, Eelco C.; Dam, Teunis J. P. van; Kops, Geert J.P.L.; Snel, Berend

doi:10.1002/bies.201900006

Cited by 16 publications

(20 citation statements)

References 94 publications

(118 reference statements)

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“…In this study, we used a remote homology detection protocol combining both profile-versus-profile and iterative HMM searches to identify highly divergent orthologues of the metazoan SYCP2:SYCP3 multimers and subunits of the KKT16 complex (figures 2 and 3 ). Specifically, we made use of the ‘hopping’ strategy, which was previously employed to detect divergent homologues of canonical kinetochore proteins [ 8 , 63 , 64 ]. The ‘hopping’ strategy uses the following logic: ‘if A is homologous to B and B is homologous to C, then A must be homologous to C’.…”

Section: Discussionmentioning

confidence: 99%

Repurposing of synaptonemal complex proteins for kinetochores in Kinetoplastida

et al. 2021

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Chromosome segregation in eukaryotes is driven by the kinetochore, a macromolecular complex that connects centromeric DNA to microtubules of the spindle apparatus. Kinetochores in well-studied model eukaryotes consist of a core set of proteins that are broadly conserved among distant eukaryotic phyla. By contrast, unicellular flagellates of the class Kinetoplastida have a unique set of 36 kinetochore components. The evolutionary origin and history of these kinetochores remain unknown. Here, we report evidence of homology between axial element components of the synaptonemal complex and three kinetoplastid kinetochore proteins KKT16-18. The synaptonemal complex is a zipper-like structure that assembles between homologous chromosomes during meiosis to promote recombination. By using sensitive homology detection protocols, we identify divergent orthologues of KKT16-18 in most eukaryotic supergroups, including experimentally established chromosomal axis components, such as Red1 and Rec10 in budding and fission yeast, ASY3-4 in plants and SYCP2-3 in vertebrates. Furthermore, we found 12 recurrent duplications within this ancient eukaryotic SYCP 2–3 gene family, providing opportunities for new functional complexes to arise, including KKT16-18 in the kinetoplastid parasite Trypanosoma brucei . We propose the kinetoplastid kinetochore system evolved by repurposing meiotic components of the chromosome synapsis and homologous recombination machinery that were already present in early eukaryotes.

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Section: Discussionmentioning

confidence: 99%

Repurposing of synaptonemal complex proteins for kinetochores in Kinetoplastida

et al. 2021

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“…There are several possible routes to test our hypotheses. One possibility is the construction of phylogenetic trees for the different proteins (domains) that could inform on the order they appeared during evolution of the polarity network (Hooff et al, 2019). Another possibility is to search for species in the current tree of life which contain intermediate steps of the evolutionary trajectory, for instance species with a more ancient version of Bem1 lacking the SH3 domain, and identify the protein self-organization principles underlying polarization in these species.…”

Section: How Evolution Might Leverage Scaffold Proteinsmentioning

confidence: 99%

Adaptability and evolution of the cell polarization machinery in budding yeast

Brauns

Cruz

et al. 2020

Preprint

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SummaryHow can a self-organized cellular function evolve, adapt to perturbations, and acquire new sub-functions? To make progress in answering these basic questions of evolutionary cell biology, we analyze, as a concrete example, the cell polarity machinery of Saccharomyces cerevisiae. This cellular module exhibits an intriguing resilience: it remains operational under genetic perturbations and recovers quickly and reproducibly from the deletion of one of its key components. Using a combination of modeling, conceptual theory, and experiments, we show that multiple, redundant self-organization mechanisms coexist within the protein network underlying cell polarization and are responsible for the module’s resilience and adaptability. Based on our mechanistic understanding of polarity establishment, we hypothesize how scaffold proteins, by introducing new connections in the existing network, can increase the redundancy of mechanisms and thus increase the evolvability of other network components. Moreover, our work suggests how a complex, redundant cellular module could have evolved from a more rudimental ancestral form.

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“…In this study we used a remote homology detection protocol combining both profile-versus-profile and iterative HMM searches to identify highly divergent orthologues of the metazoan SYCP2:SYCP3 multimers and subunits of the KKT16 complex (Figure 2, Figure 3). Specifically, we made use of the 'hopping' strategy which was previously employed to detect divergent homologues of canonical kinetochore proteins [8,61,62].…”

Section: Widespread Conservation Of the Sycp 2-3 Gene Family In Divermentioning

confidence: 99%

Repurposing of Synaptonemal Complex Proteins for Kinetochores in Kinetoplastida

Tromer

Wemyss

Waller

et al. 2021

Preprint

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Chromosome segregation in eukaryotes is driven by a macromolecular protein complex called the kinetochore that connects centromeric DNA to microtubules of the spindle apparatus. Kinetochores in well-studied model eukaryotes consist of a core set of proteins that are broadly conserved among distant eukaryotic phyla. In contrast, unicellular flagellates of the class Kinetoplastida have a unique set of kinetochore components. The evolutionary origin and history of these kinetochores remains unknown. Here, we report evidence of homology between three kinetoplastid kinetochore proteins KKT16-18 and axial element components of the synaptonemal complex, such as the SYCP2:SYCP3 multimers found in vertebrates. The synaptonemal complex is a zipper-like structure that assembles between homologous chromosomes during meiosis to promote recombination. Using a sensitive homology detection protocol, we identify divergent orthologues of SYCP2:SYCP3 in most eukaryotic supergroups including other experimentally established axial element components, such as Red1 and Rec10 in budding and fission yeast, and the ASY3:ASY4 multimers in land plants. These searches also identify KKT16-18 as part of this rapidly evolving protein family. The widespread presence of the SYCP2-3 gene family in extant eukaryotes suggests that the synaptonemal complex was likely present in the last eukaryotic common ancestor. We found at least twelve independent duplications of the SYCP2-3 gene family throughout the eukaryotic tree of life, providing opportunities for new functional complexes to arise, including KKT16-18 in Trypanosoma brucei. We propose that kinetoplastids evolved their unique kinetochore system by repurposing meiotic components of the chromosome synapsis and homologous recombination machinery that were already present in early eukaryotes.

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Inferring the Evolutionary History of Your Favorite Protein: A Guide for Molecular Biologists

Cited by 16 publications

References 94 publications

Repurposing of synaptonemal complex proteins for kinetochores in Kinetoplastida

Repurposing of synaptonemal complex proteins for kinetochores in Kinetoplastida

Adaptability and evolution of the cell polarization machinery in budding yeast

Repurposing of Synaptonemal Complex Proteins for Kinetochores in Kinetoplastida

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