Increased Sampling and Intracomplex Homologies Favor Vertical Over Horizontal Inheritance of the Dam1 Complex

Laura E van Rooijen; Eelco C Tromer; Jolien J E van Hooff; Geert J P L Kops; Berend Snel

doi:10.1093/gbe/evad017

Increased Sampling and Intracomplex Homologies Favor Vertical Over Horizontal Inheritance of the Dam1 Complex

Laura E van Rooijen, Eelco C Tromer, Jolien J E van Hooff, Geert J P L Kops, Berend Snel

Hubrecht Institute

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

2 Citations (Scopus)

Abstract

Kinetochores connect chromosomes to spindle microtubules to ensure their correct segregation during cell division. Kinetochores of human and yeasts are largely homologous, their ability to track depolymerizing microtubules, however, is carried out by the nonhomologous complexes Ska1-C and Dam1-C, respectively. We previously reported the unique anti-correlating phylogenetic profiles of Dam1-C and Ska-C found among a wide variety of eukaryotes. Based on these profiles and the limited presence of Dam1-C, we speculated that horizontal gene transfer could have played a role in the evolutionary history of Dam1-C. Here, we present an expanded analysis of Dam1-C evolution, using additional genome as well as transcriptome sequences and recently published 3D structures. This analysis revealed a wider and more complete presence of Dam1-C in Cryptista, Rhizaria, Ichthyosporea, CRuMs, and Colponemidia. The fungal Dam1-C cryo-EM structure supports earlier hypothesized intracomplex homologies, which enables the reconstruction of rooted and unrooted phylogenies. The rooted tree of concatenated Dam1-C subunits is statistically consistent with the species tree of eukaryotes, suggesting that Dam1-C is ancient, and that the present-day phylogenetic distribution is best explained by multiple, independent losses and no horizontal gene transfer was involved. Furthermore, we investigated the ancient origin of Dam1-C via profile-versus-profile searches. Homology among 8 out of the 10 Dam1-C subunits suggests that the complex largely evolved from a single multimerizing subunit that diversified into a hetero-octameric core via stepwise subunit duplication and subfunctionalization of the subunits before the origin of the last eukaryotic common ancestor.

Original language	English
Journal	Genome Biology and Evolution
Volume	15
Issue number	3
DOIs	https://doi.org/10.1093/gbe/evad017
Publication status	Published - 03 Mar 2023

Keywords

Humans
Kinetochores
Microtubule-Associated Proteins/genetics
Phylogeny
Microtubules
Cell Division
Cell Cycle Proteins/genetics
Saccharomyces cerevisiae Proteins/genetics
Chromosomal Proteins, Non-Histone/genetics

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10.1093/gbe/evad017

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title = "Increased Sampling and Intracomplex Homologies Favor Vertical Over Horizontal Inheritance of the Dam1 Complex",

abstract = "Kinetochores connect chromosomes to spindle microtubules to ensure their correct segregation during cell division. Kinetochores of human and yeasts are largely homologous, their ability to track depolymerizing microtubules, however, is carried out by the nonhomologous complexes Ska1-C and Dam1-C, respectively. We previously reported the unique anti-correlating phylogenetic profiles of Dam1-C and Ska-C found among a wide variety of eukaryotes. Based on these profiles and the limited presence of Dam1-C, we speculated that horizontal gene transfer could have played a role in the evolutionary history of Dam1-C. Here, we present an expanded analysis of Dam1-C evolution, using additional genome as well as transcriptome sequences and recently published 3D structures. This analysis revealed a wider and more complete presence of Dam1-C in Cryptista, Rhizaria, Ichthyosporea, CRuMs, and Colponemidia. The fungal Dam1-C cryo-EM structure supports earlier hypothesized intracomplex homologies, which enables the reconstruction of rooted and unrooted phylogenies. The rooted tree of concatenated Dam1-C subunits is statistically consistent with the species tree of eukaryotes, suggesting that Dam1-C is ancient, and that the present-day phylogenetic distribution is best explained by multiple, independent losses and no horizontal gene transfer was involved. Furthermore, we investigated the ancient origin of Dam1-C via profile-versus-profile searches. Homology among 8 out of the 10 Dam1-C subunits suggests that the complex largely evolved from a single multimerizing subunit that diversified into a hetero-octameric core via stepwise subunit duplication and subfunctionalization of the subunits before the origin of the last eukaryotic common ancestor.",

keywords = "Humans, Kinetochores, Microtubule-Associated Proteins/genetics, Phylogeny, Microtubules, Cell Division, Cell Cycle Proteins/genetics, Saccharomyces cerevisiae Proteins/genetics, Chromosomal Proteins, Non-Histone/genetics",

author = "{van Rooijen}, {Laura E} and Tromer, {Eelco C} and {van Hooff}, {Jolien J E} and Kops, {Geert J P L} and Berend Snel",

note = "{\textcopyright} The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.",

year = "2023",

month = mar,

day = "3",

doi = "10.1093/gbe/evad017",

language = "English",

volume = "15",

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T1 - Increased Sampling and Intracomplex Homologies Favor Vertical Over Horizontal Inheritance of the Dam1 Complex

AU - van Rooijen, Laura E

AU - Tromer, Eelco C

AU - van Hooff, Jolien J E

AU - Kops, Geert J P L

AU - Snel, Berend

N1 - © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

PY - 2023/3/3

Y1 - 2023/3/3

N2 - Kinetochores connect chromosomes to spindle microtubules to ensure their correct segregation during cell division. Kinetochores of human and yeasts are largely homologous, their ability to track depolymerizing microtubules, however, is carried out by the nonhomologous complexes Ska1-C and Dam1-C, respectively. We previously reported the unique anti-correlating phylogenetic profiles of Dam1-C and Ska-C found among a wide variety of eukaryotes. Based on these profiles and the limited presence of Dam1-C, we speculated that horizontal gene transfer could have played a role in the evolutionary history of Dam1-C. Here, we present an expanded analysis of Dam1-C evolution, using additional genome as well as transcriptome sequences and recently published 3D structures. This analysis revealed a wider and more complete presence of Dam1-C in Cryptista, Rhizaria, Ichthyosporea, CRuMs, and Colponemidia. The fungal Dam1-C cryo-EM structure supports earlier hypothesized intracomplex homologies, which enables the reconstruction of rooted and unrooted phylogenies. The rooted tree of concatenated Dam1-C subunits is statistically consistent with the species tree of eukaryotes, suggesting that Dam1-C is ancient, and that the present-day phylogenetic distribution is best explained by multiple, independent losses and no horizontal gene transfer was involved. Furthermore, we investigated the ancient origin of Dam1-C via profile-versus-profile searches. Homology among 8 out of the 10 Dam1-C subunits suggests that the complex largely evolved from a single multimerizing subunit that diversified into a hetero-octameric core via stepwise subunit duplication and subfunctionalization of the subunits before the origin of the last eukaryotic common ancestor.

AB - Kinetochores connect chromosomes to spindle microtubules to ensure their correct segregation during cell division. Kinetochores of human and yeasts are largely homologous, their ability to track depolymerizing microtubules, however, is carried out by the nonhomologous complexes Ska1-C and Dam1-C, respectively. We previously reported the unique anti-correlating phylogenetic profiles of Dam1-C and Ska-C found among a wide variety of eukaryotes. Based on these profiles and the limited presence of Dam1-C, we speculated that horizontal gene transfer could have played a role in the evolutionary history of Dam1-C. Here, we present an expanded analysis of Dam1-C evolution, using additional genome as well as transcriptome sequences and recently published 3D structures. This analysis revealed a wider and more complete presence of Dam1-C in Cryptista, Rhizaria, Ichthyosporea, CRuMs, and Colponemidia. The fungal Dam1-C cryo-EM structure supports earlier hypothesized intracomplex homologies, which enables the reconstruction of rooted and unrooted phylogenies. The rooted tree of concatenated Dam1-C subunits is statistically consistent with the species tree of eukaryotes, suggesting that Dam1-C is ancient, and that the present-day phylogenetic distribution is best explained by multiple, independent losses and no horizontal gene transfer was involved. Furthermore, we investigated the ancient origin of Dam1-C via profile-versus-profile searches. Homology among 8 out of the 10 Dam1-C subunits suggests that the complex largely evolved from a single multimerizing subunit that diversified into a hetero-octameric core via stepwise subunit duplication and subfunctionalization of the subunits before the origin of the last eukaryotic common ancestor.

KW - Humans

KW - Kinetochores

KW - Microtubule-Associated Proteins/genetics

KW - Phylogeny

KW - Microtubules

KW - Cell Division

KW - Cell Cycle Proteins/genetics

KW - Saccharomyces cerevisiae Proteins/genetics

KW - Chromosomal Proteins, Non-Histone/genetics

U2 - 10.1093/gbe/evad017

DO - 10.1093/gbe/evad017

M3 - Article

C2 - 36790109

SN - 1759-6653

VL - 15

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

IS - 3

ER -

Increased Sampling and Intracomplex Homologies Favor Vertical Over Horizontal Inheritance of the Dam1 Complex

Abstract

Keywords

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