Neocentromeres Provide Chromosome Segregation Accuracy and Centromere Clustering to Multiple Loci along a Candida albicans Chromosome

Burrack, Laura S.; Hutton, Hannah F.; Matter, Kathleen J.; Clancey, Shelly Applen; Liachko, Ivan; Plemmons, Alexandra E.; Saha, Amrita; Power, Erica A; Turman, Breanna J.; Thevandavakkam, Mathuravani A.; Ay, Ferhat; Dunham, Maitreya J.; Berman, Judith

doi:10.1371/journal.pgen.1006317

“…'Centromere repositioning', that is, the movement of the centromere along the chromosome without marker order variation, was first given as a possible mechanism for karyotype evolution in a broad investigation of chromosomal evolution in 60 species of primates (Dutrillaux 1979). Over the past few decades, numerous studies have found evolutionary new centromeres in different lineages, including fungi, insects, birds, and mammals (O'Neill et al 2004;Marshall et al 2008;Rocchi et al 2012;Scott and Sullivan 2014;Schneider et al 2016;Burrack et al 2016;Tolomeo et al 2017). Some of the observed karyotype reshuffling may be due to the inheritance of neo-centromeres (Amor et al 2004) while some may be the product of successive pericentric inversions (Rocchi et al 2012).…”

Section: Discussionmentioning

confidence: 99%

Dynamic turnover of centromeres drives karyotype evolution in Drosophila

Bracewell

¹

,

Chatla

²

,

Nalley

³

et al. 2019

Preprint

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Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high--quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene--rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat--content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

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“…Neocentromeres are previously naïve chromatin regions that give rise to functional kinetochores competent for chromosome segregation. Upon inactivation or deletion of the original centromeres, Candida neocentromeres form almost anywhere on the chromosome, though there is some preference for transcriptionally silent pericentric and subtelomeric regions [43, 210–212]. Like in S. cerevisiae , centromeres and neocentromeres in Candida interfere with transcription of nearby genes [210], also suggesting heterochromatin characteristics.…”

Section: Chromosome Landmarks: Origins Telomeres and Centromeresmentioning

confidence: 99%

“…Upon inactivation or deletion of the original centromeres, Candida neocentromeres form almost anywhere on the chromosome, though there is some preference for transcriptionally silent pericentric and subtelomeric regions [43, 210–212]. Like in S. cerevisiae , centromeres and neocentromeres in Candida interfere with transcription of nearby genes [210], also suggesting heterochromatin characteristics. The role of histone modifications for centrochromatin in Candida is unresolved; like S. cerevisiae, Candida lacks the conserved heterochromatin pathways that rely on methylation of H3K9 and H3K27.…”

Section: Chromosome Landmarks: Origins Telomeres and Centromeresmentioning

confidence: 99%

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

Erlendson

¹

,

Friedman

²

,

Freitag

³

2017

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Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Aspergillus nidulans and Neurospora crassa. Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of “accessory” or “conditionally dispensable” chromosomes, and contrast what has been learned from studies on genome-wide chromosome conformation capture in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Neurospora crassa and Trichoderma reesei. While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology and evolutionary biology.

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“…Neocentromeres are previously naïve chromatin regions that give rise to functional kinetochores competent for chromosome segregation. Upon inactivation or deletion of the original centromeres, Candida neocentromeres form almost anywhere on the chromosome, though there is some preference for transcriptionally silent pericentric and subtelomeric regions [43,[210][211][212]. Like in S. cerevisiae, centromeres and neocentromeres in Candida interfere with transcription of nearby genes [210], also suggesting heterochromatin characteristics.…”

Section: Author Manuscriptmentioning

confidence: 99%

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

Erlendson

¹

,

Friedman

²

,

Freitag

³

2017

View full text Add to dashboard Cite

Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Aspergillus nidulans and Neurospora crassa. Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of "accessory" or "conditionally dispensable" chromosomes, and contrast what has been learned from studies on genome-wide chromosome conformation capture in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Neurospora crassa and Trichoderma reesei. While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology and evolutionary biology. CHROMATIN: AN ASSEMBLY OF DNA, PROTEINS, AND RNAChromosomes of fungi are linear segments of DNA, covered by a diverse assembly of RNA and proteins. They contain three landmarks required for function, namely origins for DNA replication, centromeric DNA as attachment points for kinetochores and telomere repeats to circumvent the end replication problem for linear DNA. Because fungi have been excellent model organisms for trail-blazing basic research since the adoption of Neurospora crassa as one of the workhorses for genetics in the 1940s [1], much of the foundation for general knowledge of eukaryotes was first uncovered with fungi, specifically the four species uniquely suited for genetics, biochemistry and genomics, Schizosaccharomyces pombe, Saccharomyces cerevisiae, Aspergillus nidulans, and N. crassa. This has certainly also been true for studies on chromatin and chromosomes.Chromatin, the building material for chromosomes, is an assembly of DNA, proteins and RNA, organized into nucleosome units, most of which contain octamers of canonical core histone proteins [2]. The three landmarks on chromosomes mentioned above, origins of replication, telomeres and centromeres, are characterized by different specialized chromatin modifications, for example DNA base modifications, like cytosine or adenine methylation, and posttranslational modifications of histones, and it is the set of gene silencing modifications at those chromosome landmarks that will be examined here in more detail. Occupancy of proteins binding spec...

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Neocentromeres Provide Chromosome Segregation Accuracy and Centromere Clustering to Multiple Loci along a Candida albicans Chromosome

Cited by 37 publications

References 66 publications

Dynamic turnover of centromeres drives karyotype evolution in Drosophila

Dynamic turnover of centromeres drives karyotype evolution in Drosophila

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

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