Co-evolving CENP-A and CAL1 Domains Mediate Centromeric CENP-A Deposition across Drosophila Species

Rosin, Leah F.; Mellone, Barbara G.

doi:10.1016/j.devcel.2016.03.021

Cited by 41 publications

(57 citation statements)

References 61 publications

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“…Alternatively, other centromere-associated protein(s) may provide DNA-sequence specificity and evolve to suppress centromere drive Malik and Henikoff 2009). Adaptive evolution of CENH3 could in turn be driven by its interaction with these proteins, for example CENP-C, or instead be driven by modulation of its centromere deposition efficiency through its loading factor as proposed for Drosophila (Rosin and Mellone 2016).…”

Section: Discussionmentioning

confidence: 99%

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

et al. 2017

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During cell division, spindle fibers attach to chromosomes at centromeres. The DNA sequence at regional centromeres is fast evolving with no conserved genetic signature for centromere identity. Instead CENH3, a centromere-specific histone H3 variant, is the epigenetic signature that specifies centromere location across both plant and animal kingdoms. Paradoxically, CENH3 is also adaptively evolving. An ongoing question is whether CENH3 evolution is driven by a functional relationship with the underlying DNA sequence. Here, we demonstrate that despite extensive protein sequence divergence, CENH3 histones from distant species assemble centromeres on the same underlying DNA sequence. We first characterized the organization and diversity of centromere repeats in wild-type Arabidopsis thaliana. We show that A. thaliana CENH3-containing nucleosomes exhibit a strong preference for a unique subset of centromeric repeats. These sequences are largely missing from the genome assemblies and represent the youngest and most homogeneous class of repeats. Next, we tested the evolutionary specificity of this interaction in a background in which the native A. thaliana CENH3 is replaced with CENH3s from distant species. Strikingly, we find that CENH3 from Lepidium oleraceum and Zea mays, although specifying epigenetically weaker centromeres that result in genome elimination upon outcrossing, show a binding pattern on A. thaliana centromere repeats that is indistinguishable from the native CENH3. Our results demonstrate positional stability of a highly diverged CENH3 on independently evolved repeats, suggesting that the sequence specificity of centromeres is determined by a mechanism independent of CENH3.

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Section: Discussionmentioning

confidence: 99%

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

et al. 2017

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“…Functional orthologs with limited sequence similarity to HJURP exist in S. cerevisiae , S. pombe , and D. melanogaster (named Scm3 and Cal1) [369,370,371,372,373,374,375,376,377,378,379]. HJURP, which may form functional dimers [380], contains an N-terminal Scm3-homology domain that binds pre-nucleosomal CENP-A [73,75,158,381,382,383,384].…”

Section: The Propagation Of Centromeric Chromatinmentioning

confidence: 99%

A Molecular View of Kinetochore Assembly and Function

Musacchio

Desai

2017

Biology

477

589

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Kinetochores are large protein assemblies that connect chromosomes to microtubules of the mitotic and meiotic spindles in order to distribute the replicated genome from a mother cell to its daughters. Kinetochores also control feedback mechanisms responsible for the correction of incorrect microtubule attachments, and for the coordination of chromosome attachment with cell cycle progression. Finally, kinetochores contribute to their own preservation, across generations, at the specific chromosomal loci devoted to host them, the centromeres. They achieve this in most species by exploiting an epigenetic, DNA-sequence-independent mechanism; notable exceptions are budding yeasts where a specific sequence is associated with centromere function. In the last 15 years, extensive progress in the elucidation of the composition of the kinetochore and the identification of various physical and functional modules within its substructure has led to a much deeper molecular understanding of kinetochore organization and the origins of its functional output. Here, we provide a broad summary of this progress, focusing primarily on kinetochores of humans and budding yeast, while highlighting work from other models, and present important unresolved questions for future studies.

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“…Importantly, in either situation (Figure 3BI–II), modulating CENP-A binding could also be accomplished by CENP-A alleles that somehow alter CENP-A’s deposition by its chaperone [113], as discussed below.…”

Section: Models Of How Cenp-a Could Suppress Centromere Drivementioning

confidence: 99%

“…This work showed that the presence of an evolutionarily compatible CAL1 partner is the only requirement for centromeric targeting, even across large evolutionary distances where the centromeric DNA sequences have presumably diverged (Figure 4A; [113]).…”

Section: The Presence Of Species-matched Cenp-a and Cal1 Allows Cenp-mentioning

confidence: 99%

Centromeres Drive a Hard Bargain

Rosin

Mellone

2017

Trends in Genetics

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Centromeres are essential chromosomal structures that mediate the accurate distribution of genetic material during meiotic and mitotic cell divisions. In most organisms, centromeres are epigenetically specified and propagated by nucleosomes containing the centromere-specific H3 variant, CENP-A. Although centromeres perform a critical and conserved function, CENP-A and the underlying centromeric DNA are rapidly evolving. This paradox has been explained by the centromere drive hypothesis, which proposes that CENP-A is undergoing an evolutionary tug-of-war with selfish centromeric DNA. Here, we review our current understanding of CENP-A evolution in relation to centromere drive and discuss classical and recent advances, including new evidence implicating CENP-A chaperones in this conflict.

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Co-evolving CENP-A and CAL1 Domains Mediate Centromeric CENP-A Deposition across Drosophila Species

Cited by 41 publications

References 61 publications

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

A Molecular View of Kinetochore Assembly and Function

Centromeres Drive a Hard Bargain

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