scholarly journals Adaptive Evolution of Cid, a Centromere-Specific Histone in Drosophila

Genetics ◽  
2001 ◽  
Vol 157 (3) ◽  
pp. 1293-1298 ◽  
Author(s):  
Harmit S Malik ◽  
Steven Henikoff

Abstract Centromeric DNA is generally composed of large blocks of tandem satellite repeats that change rapidly due to loss of old arrays and expansion of new repeat classes. This extreme heterogeneity of centromeric DNA is difficult to reconcile with the conservation of the eukaryotic chromosome segregation machinery. Histone H3-like proteins, including Cid in Drosophila melanogaster, are a unique chromatin component of centromeres. In comparisons between closely related species of Drosophila, we find an excess of replacement changes that have been fixed since the separation of D. melanogaster and D. simulans, suggesting adaptive evolution. The last adaptive changes appear to have occurred recently, as evident from a reduction in polymorphism in the melanogaster lineage. Adaptive evolution has occurred both in the long N-terminal tail as well as in the histone fold of Cid. In the histone fold, the replacement changes have occurred in the region proposed to mediate binding to DNA. We propose that this rapid evolution of Cid is driven by a response to the changing satellite repeats at centromeres. Thus, centromeric H3-like proteins may act as adaptors between evolutionarily labile centromeric DNA and the conserved kinetochore machinery.

2018 ◽  
Author(s):  
Cedric A. Brimacombe ◽  
Jordan E. Burke ◽  
Jahan-Yar Parsa ◽  
Jessica N. Witchley ◽  
Laura S. Burrack ◽  
...  

Eukaryotes have evolved elaborate mechanisms to ensure that chromosomes segregate with high fidelity during mitosis and meiosis1, and yet specific aneuploidies can be adaptive during environmental stress2,3. Here, we identify a chromatin-based system for inducible aneuploidy in a human pathogen. Candida albicans utilizes chromosome missegregation to acquire resistance to antifungal drugs4,5 and for ploidy reduction after mating6. We discovered that the ancestor of C. albicans and two related pathogens evolved a variant of histone H2A that lacks the conserved phosphorylation site for Bub1 kinase7, a key regulator of chromosome segregation1. Expression of this variant controls the rates of aneuploidy and antibiotic resistance in this species. Moreover, CENP-A/Cse4, the histone H3 that specifies centromeres, is depleted from tetraploid mating products and virtually eliminated from cells exposed to aneuploidy-promoting cues. Thus, changes in chromatin regulation can confer the capacity for rapid evolution in eukaryotes.


2002 ◽  
Vol 22 (21) ◽  
pp. 7553-7561 ◽  
Author(s):  
Danielle Vermaak ◽  
Hillary S. Hayden ◽  
Steven Henikoff

ABSTRACT Centromeres require specialized nucleosomes; however, the mechanism of localization is unknown. Drosophila sp. centromeric nucleosomes contain the Cid H3-like protein. We have devised a strategy for identifying elements within Cid responsible for its localization to centromeres. By expressing Cid from divergent Drosophila species fused to green fluorescent protein in Drosophila melanogaster cells, we found that D. bipectinata Cid fails to localize to centromeres. Cid chimeras consisting of the D. bipectinata histone fold domain (HFD) replaced with segments from D. melanogaster identified loop I of the HFD as being critical for targeting to centromeres. Conversely, substitution of D. bipectinata loop I into D. melanogaster abolished centromeric targeting. In either case, loop I was the only segment capable of conferring targeting. Within loop I, we identified residues that are critical for targeting. Most mutations of conserved residues abolished targeting, and length reductions were deleterious. Taken together with the fact that H3 loop I makes numerous contacts with DNA and with the adaptive evolution of Cid, our results point to the importance of DNA specificity for targeting. We suggest that the process of deposition of (Cid.H4)2 tetramers allows for discriminating contacts to be made between loop I and DNA, providing the specificity needed for targeting.


2016 ◽  
Vol 44 (5) ◽  
pp. 1201-1217 ◽  
Author(s):  
Bungo Akiyoshi

The kinetochore is the macromolecular protein complex that drives chromosome segregation in eukaryotes. Its most fundamental function is to connect centromeric DNA to dynamic spindle microtubules. Studies in popular model eukaryotes have shown that centromere protein (CENP)-A is critical for DNA-binding, whereas the Ndc80 complex is essential for microtubule-binding. Given their conservation in diverse eukaryotes, it was widely believed that all eukaryotes would utilize these components to make up a core of the kinetochore. However, a recent study identified an unconventional type of kinetochore in evolutionarily distant kinetoplastid species, showing that chromosome segregation can be achieved using a distinct set of proteins. Here, I review the discovery of the two kinetochore systems and discuss how their studies contribute to a better understanding of the eukaryotic chromosome segregation machinery.


2005 ◽  
Vol 16 (12) ◽  
pp. 5649-5660 ◽  
Author(s):  
Kimberly A. Collins ◽  
Andrea R. Castillo ◽  
Sean Y. Tatsutani ◽  
Sue Biggins

Kinetochores mediate chromosome attachment to the mitotic spindle to ensure accurate chromosome segregation. Budding yeast is an excellent organism for kinetochore assembly studies because it has a simple defined centromere sequence responsible for the localization of >65 proteins. In addition, yeast is the only organism where a conditional centromere is available to allow studies of de novo kinetochore assembly. Using a conditional centromere, we found that yeast kinetochore assembly is not temporally restricted and can occur in both G1 phase and prometaphase. We performed the first investigation of kinetochore assembly in the absence of the centromeric histone H3 variant Cse4 and found that all proteins tested depend on Cse4 to localize. Consistent with this observation, Cse4-depleted cells had severe chromosome segregation defects. We therefore propose that yeast kinetochore assembly requires both centromeric DNA specificity and centromeric chromatin.


Open Biology ◽  
2016 ◽  
Vol 6 (3) ◽  
pp. 150206 ◽  
Author(s):  
Olga O. Nerusheva ◽  
Bungo Akiyoshi

Kinetochores are macromolecular machines that drive eukaryotic chromosome segregation by interacting with centromeric DNA and spindle microtubules. While most eukaryotes possess conventional kinetochore proteins, evolutionarily distant kinetoplastid species have unconventional kinetochore proteins, composed of at least 19 proteins (KKT1–19). Polo-like kinase (PLK) is not a structural kinetochore component in either system. Here, we report the identification of an additional kinetochore protein, KKT20, in Trypanosoma brucei . KKT20 has sequence similarity with KKT2 and KKT3 in the Cys-rich region, and all three proteins have weak but significant similarity to the polo box domain (PBD) of PLK. These divergent PBDs of KKT2 and KKT20 are sufficient for kinetochore localization in vivo . We propose that the ancestral PLK acquired a Cys-rich region and then underwent gene duplication events to give rise to three structural kinetochore proteins in kinetoplastids.


2018 ◽  
Vol 115 (12) ◽  
pp. 3108-3113 ◽  
Author(s):  
Vikas Yadav ◽  
Sheng Sun ◽  
R. Blake Billmyre ◽  
Bhagya C. Thimmappa ◽  
Terrance Shea ◽  
...  

The centromere DNA locus on a eukaryotic chromosome facilitates faithful chromosome segregation. Despite performing such a conserved function, centromere DNA sequence as well as the organization of sequence elements is rapidly evolving in all forms of eukaryotes. The driving force that facilitates centromere evolution remains an enigma. Here, we studied the evolution of centromeres in closely related species in the fungal phylum of Basidiomycota. Using ChIP-seq analysis of conserved inner kinetochore proteins, we identified centromeres in three closely related Cryptococcus species: two of which are RNAi-proficient, while the other lost functional RNAi. We find that the centromeres in the RNAi-deficient species are significantly shorter than those of the two RNAi-proficient species. While centromeres are LTR retrotransposon-rich in all cases, the RNAi-deficient species lost all full-length retroelements from its centromeres. In addition, centromeres in RNAi-proficient species are associated with a significantly higher level of cytosine DNA modifications compared with those of RNAi-deficient species. Furthermore, when an RNAi-proficient Cryptococcus species and its RNAi-deficient mutants were passaged under similar conditions, the centromere length was found to be occasionally shortened in RNAi mutants. In silico analysis of predicted centromeres in a group of closely related Ustilago species, also belonging to the Basidiomycota, were found to have undergone a similar transition in the centromere length in an RNAi-dependent fashion. Based on the correlation found in two independent basidiomycetous species complexes, we present evidence suggesting that the loss of RNAi and cytosine DNA methylation triggered transposon attrition, which resulted in shortening of centromere length during evolution.


Genetics ◽  
2003 ◽  
Vol 163 (1) ◽  
pp. 447-452 ◽  
Author(s):  
Jeffrey S Thompson ◽  
Marilyn L Snow ◽  
Summer Giles ◽  
Leslie E McPherson ◽  
Michael Grunstein

Abstract Fourteen novel single-amino-acid substitution mutations in histone H3 that disrupt telomeric silencing in Saccharomyces cerevisiae were identified, 10 of which are clustered within the α1 helix and L1 loop of the essential histone fold. Several of these mutations cause derepression of silent mating locus HML, and an additional subset cause partial loss of basal repression at the GAL1 promoter. Our results identify a new domain within the essential core of histone H3 that is required for heterochromatin-mediated silencing.


2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Patrick M. Ferree ◽  
Satyaki Prasad

Satellites are one of the most enigmatic parts of the eukaryotic genome. These highly repetitive, noncoding sequences make up as much as half or more of the genomic content and are known to play essential roles in chromosome segregation during meiosis and mitosis, yet they evolve rapidly between closely related species. Research over the last several decades has revealed that satellite divergence can serve as a formidable reproductive barrier between sibling species. Here we highlight several key studies on Drosophila and other model organisms demonstrating deleterious effects of satellites and their rapid evolution on the structure and function of chromosomes in interspecies hybrids. These studies demonstrate that satellites can impact chromosomes at a number of different developmental stages and through distinct cellular mechanisms, including heterochromatin formation. These findings have important implications for how loci that cause postzygotic reproductive isolation are viewed.


2003 ◽  
Vol 12 (5) ◽  
pp. 1277-1285 ◽  
Author(s):  
David D. Duvernell ◽  
Paul S. Schmidt ◽  
Walter F. Eanes

Sign in / Sign up

Export Citation Format

Share Document