Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in <i>Candida albicans</i>

Thakur, Jitendra; Sanyal, Kaustuv

doi:10.1101/gr.141614.112

Cited by 80 publications

(121 citation statements)

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“…The conditions for de novo centromere formation remain unclear (26). Recent research revealed that many de novo centromeres prefer to form near native centromeric regions or in the heterochromatic regions, such as the pericentromere and telomere (27,28). There are also de novo centromeres in human formed far from native centromeres (20).…”

Section: Significancementioning

confidence: 99%

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Liu

Pang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The ability of centromeres to alternate between active and inactive states indicates significant epigenetic aspects controlling centromere assembly and function. In maize (Zea mays), misdivision of the B chromosome centromere on a translocation with the short arm of chromosome 9 (TB-9Sb) can produce many variants with varying centromere sizes and centromeric DNA sequences. In such derivatives of TB-9Sb, we found a de novo centromere on chromosome derivative 3-3, which has no canonical centromeric repeat sequences. This centromere is derived from a 288-kb region on the short arm of chromosome 9, and is 19 megabases (Mb) removed from the translocation breakpoint of chromosome 9 in TB-9Sb. The functional B centromere in progenitor telo2-2 is deleted from derivative 3-3, but some B-repeat sequences remain. The de novo centromere of derivative 3-3 becomes inactive in three further derivatives with new centromeres being formed elsewhere on each chromosome. Our results suggest that de novo centromere initiation is quite common and can persist on chromosomal fragments without a canonical centromere. However, we hypothesize that when de novo centromeres are initiated in opposition to a larger normal centromere, they are cleared from the chromosome by inactivation, thus maintaining karyotype integrity.centromere misdivision | epigenetics | de novo centromere | centromere inactivation T he centromere is an important chromosomal region responsible for correct chromosome segregation during cell division. Centromeres are found in the primary constriction region on the chromosome, upon which the kinetochore complex assembles to produce a platform for spindle binding (1). Centromere function is conserved among different species, and several epigenetic markers of active centromeres have been found, including a histone H3 variant referred to as CENH3 in plants (2, 3) or CENP-A in animals (4-6) and phosphorylation of histone H2A at Thr133 in plants (7). Correct loading of CENH3 to the centromere region is a key component of kinetochore assembly (8). Centromeric DNA sequences have experienced rapid evolution (9, 10), and arrangements of DNA sequence in centromere regions differ in species and even in different chromosomes of an individual organism (11). Myriad repeat sequences exist in the centromeres of higher plants. In maize (Zea mays), there are two major types of centromere specific DNA sequences: the simple satellite repeat sequence CentC (12) and centromeric retrotransposon of maize (CRM) (3). Many epigenetic features have been identified in centromeric regions, including DNA methylation levels, histone variants, histone modifications, and RNA components (11). Both epigenetic elements and DNA sequences take part in centromere formation and maintenance, but it is still unknown how genetic and epigenetic factors work together in this process.The centromere is one of the most complex regions on the chromosome, and complete DNA sequencing through the centromeric region is difficult to obtain due to their highly repetitive nature...

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Section: Significancementioning

confidence: 99%

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Liu

Pang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…In C. albicans (yeast) and Gallus gallus (chicken) DT40 cells, new centromeres were found in several positions, most frequently close to the original centromere (141, 154). It is thought that low levels of CENP-A in regions flanking the centromere may seed these new centromeres.…”

Section: Introductionmentioning

confidence: 99%

“…The absence of satellite sequences in neocentromeres is indicative of their nonessential centromere function. The conclusion from a phylogenetically broad spectrum of plants and animals indicates that there are neocentromere-favorable and -unfavorable sites (154, 161). Unlike the kinetochore, with its readily identifiable essential proteins, it is difficult (outside of budding yeast) to identify genetic sequences or modifications that definitively mark or exclude centromere formation.…”

Section: Introductionmentioning

confidence: 99%

Centromeric Heterochromatin: The Primordial Segregation Machine

Bloom

2014

Annu. Rev. Genet.

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Centromeres are specialized domains of heterochromatin that provide the foundation for the kinetochore. Centromeric heterochromatin is characterized by specific histone modifications, a centromere-specific histone H3 variant (CENP-A), and the enrichment of cohesin, condensin, and topo-isomerase II. Centromere DNA varies orders of magnitude in size from 125 bp (budding yeast) to several megabases (human). In metaphase, sister kinetochores on the surface of replicated chromosomes face away from each other, where they establish microtubule attachment and bi-orientation. Despite the disparity in centromere size, the distance between separated sister kinetochores is remarkably conserved (approximately 1 μm) throughout phylogeny. The centromere functions as a molecular spring that resists microtubule-based extensional forces in mitosis. This review explores the physical properties of DNA in order to understand how the molecular spring is built and how it contributes to the fidelity of chromosome segregation.

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“…The hybrid condition did not reposition the centromeres, even though neocentromeres have a high propensity to be formed in C. albicans chromosomes (34). ChIP analysis revealed that the centromere location of chromosome 4 changed between two C. dubliniensis strains, Cd36 (19) and CdUM4b.…”

Section: Discussionmentioning

confidence: 95%

A Stable Hybrid Containing Haploid Genomes of Two Obligate Diploid Candida Species

Chakraborty

Aiyaz²,

Kakade

et al. 2013

Eukaryot Cell

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Candida albicans and Candida dubliniensis are diploid, predominantly asexual human-pathogenic yeasts. In this study, we constructed tetraploid (4n) strains of C. albicans of the same or different lineages by spheroplast fusion. Induction of chromosome loss in the tetraploid C. albicans generated diploid or near-diploid progeny strains but did not produce any haploid progeny. We also constructed stable heterotetraploid somatic hybrid strains (2n ؉ 2n) of C. albicans and C. dubliniensis by spheroplast fusion. Heterodiploid (n ؉ n) progeny hybrids were obtained after inducing chromosome loss in a stable heterotetraploid hybrid. To identify a subset of hybrid heterodiploid progeny strains carrying at least one copy of all chromosomes of both species, unique centromere sequences of various chromosomes of each species were used as markers in PCR analysis. The reduction of chromosome content was confirmed by a comparative genome hybridization (CGH) assay. The hybrid strains were found to be stably propagated. Chromatin immunoprecipitation (ChIP) assays with antibodies against centromere-specific histones (C. albicans Cse4/C. dubliniensis Cse4) revealed that the centromere identity of chromosomes of each species is maintained in the hybrid genomes of the heterotetraploid and heterodiploid strains. Thus, our results suggest that the diploid genome content is not obligatory for the survival of either C. albicans or C. dubliniensis. In keeping with the recent discovery of the existence of haploid C. albicans strains, the heterodiploid strains of our study can be excellent tools for further species-specific genome elimination, yielding true haploid progeny of C. albicans or C. dubliniensis in future.

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Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans

Cited by 80 publications

References 58 publications

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Centromeric Heterochromatin: The Primordial Segregation Machine

A Stable Hybrid Containing Haploid Genomes of Two Obligate Diploid Candida Species

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