Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome

Villasanté, Alfredo; Abad, José Pascual; Méndez-Lago, María

doi:10.1073/pnas.0703808104

Cited by 80 publications

(72 citation statements)

References 115 publications

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“…One of the striking observations from that study is the role of telomere-proximal regions in serving the platform for centromere formation. This may support the hypothesis that centromeres originated from telomeres during karyotype evolution (132).…”

Section: The Neocentromere: Formation Of a Centromere On A Nonnative supporting

confidence: 77%

Diversity in Requirement of Genetic and Epigenetic Factors for Centromere Function in Fungi

Roy

Sanyal

2011

Eukaryot Cell

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A centromere is a chromosomal region on which several proteins assemble to form the kinetochore. The centromere-kinetochore complex helps in the attachment of chromosomes to spindle microtubules to mediate segregation of chromosomes to daughter cells during mitosis and meiosis. In several budding yeast species, the centromere forms in a DNA sequence-dependent manner, whereas in most other fungi, factors other than the DNA sequence also determine the centromere location, as centromeres were able to form on nonnative sequences (neocentromeres) when native centromeres were deleted in engineered strains. Thus, in the absence of a common DNA sequence, the cues that have facilitated centromere formation on a specific DNA sequence for millions of years remain a mystery. Kinetochore formation is facilitated by binding of a centromere-specific histone protein member of the centromeric protein A (CENP-A) family that replaces a canonical histone H3 to form a specialized centromeric chromatin structure. However, the process of kinetochore formation on the rapidly evolving and seemingly diverse centromere DNAs in different fungal species is largely unknown. More interestingly, studies in various yeasts suggest that the factors required for de novo centromere formation (establishment) may be different from those required for maintenance (propagation) of an already established centromere. Apart from the DNA sequence and CENP-A, many other factors, such as posttranslational modification (PTM) of histones at centric and pericentric chromatin, RNA interference, and DNA methylation, are also involved in centromere formation, albeit in a species-specific manner. In this review, we discuss how several genetic and epigenetic factors influence the evolution of structure and function of centromeres in fungal species.A complete understanding of the complexities of the process of cellular differentiation requires a thorough analysis of the molecular events occurring during eukaryotic cell division. As an important part of this process, a cell has to ensure accurate segregation of duplicated chromosomes into its progeny cells. In eukaryotes, specific DNA sequences, and the factors that bind to them immediately after replication, partly dictate the state of chromatin. Apart from the genetic factors, many epigenetic phenomena also contribute to formation of specialized chromatin required for specific functions. One such specialized chromatin domain, the centromere (CEN)-kinetochore complex, plays a crucial role in high-fidelity chromosome segregation and has great implications for human health. A consequence of improper chromosome segregation is the abnormal chromosome numbers associated with most human cancers. For example, in human colorectal cancers, almost 85% of cells are aneuploid, with 60 to 90 chromosomes (128).The high-fidelity chromosome segregation that occurs during mitosis and meiosis requires a functional centromere, defined as the primary constriction on a chromosome. The centromere is a region where spindle fibers attach to ...

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Section: The Neocentromere: Formation Of a Centromere On A Nonnative supporting

confidence: 77%

Diversity in Requirement of Genetic and Epigenetic Factors for Centromere Function in Fungi

Roy

Sanyal

2011

Eukaryot Cell

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“…Subtelomeric repetitive sequences and/or SD could have a role in these exchanges. We can also note that Villasante et al (2007) have proposed that, during the evolution of eukaryotic chromosomes, the centromeres were derived from telomeres.…”

Section: Enc Evolutionary Modifications After Seedingmentioning

confidence: 99%

Centromere repositioning in mammals

et al. 2011

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The evolutionary history of chromosomes can be tracked by the comparative hybridization of large panels of bacterial artificial chromosome clones. This approach has disclosed an unprecedented phenomenon: 'centromere repositioning', that is, the movement of the centromere along the chromosome without marker order variation. The occurrence of evolutionary new centromeres (ENCs) is relatively frequent. In macaque, for instance, 9 out of 20 autosomal centromeres are evolutionarily new; in donkey at least 5 such neocentromeres originated after divergence from the zebra, in less than 1 million years. Recently, orangutan chromosome 9, considered to be heterozygous for a complex rearrangement, was discovered to be an ENC. In humans, in addition to neocentromeres that arise in acentric fragments and result in clinical phenotypes, 8 centromererepositioning events have been reported. These 'real-time' repositioned centromere-seeding events provide clues to ENC birth and progression. In the present paper, we provide a review of the centromere repositioning. We add new data on the population genetics of the ENC of the orangutan, and describe for the first time an ENC on the X chromosome of squirrel monkeys. Next-generation sequencing technologies have started an unprecedented, flourishing period of rapid whole-genome sequencing. In this context, it is worth noting that these technologies, uncoupled from cytogenetics, would miss all the biological data on evolutionary centromere repositioning. Therefore, we can anticipate that classical and molecular cytogenetics will continue to have a crucial role in the identification of centromere movements. Indeed, all ENCs and human neocentromeres were found following classical and molecular cytogenetic investigations. Heredity (2012) 108, 59-67; doi:10.1038/hdy.2011.101; published online 2 November 2011 Keywords: neocentromeres; mammals; centromere movements; evolutionary new centromeres; evolution INTRODUCTIONThe centromere is a complex chromosomal structure responsible for proper chromosome/chromatid segregation at meiosis and mitosis. In almost all eukaryotes, centromeres are found at specific locations along chromosomes and are composed of, occasionally very large, blocks of satellite DNA. Evidence shows that in spite of the very high conservation of centromeric proteins (CENP), the satellite DNA sequences can substantially differ even among closely related species. Recently, two interconnected phenomena, human neocentromeres (HN) and evolutionary new centromeres (ENC, also called repositioned centromeres), have revolutionized our understanding of centromere function and its relationship to the underlining DNA sequences. HNs are centromeres that emerge in ectopic chromosomal regions and are devoid of alphoid sequences, that is, the satellite DNA present at primate centromeres. ENCs are centromeres that move to a new position along the chromosome without any change in marker order (no inversion or other structural rearrangements).

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“…85 In fact, it has been proposed that centromeres evolved from telomeres. 86 (2) Resident repair proteins could ensure the assembly of CENP-A and its associated proteins during every cell cycle by an endogenous DNA cutting mechanism. This would be analogous to how antibody class-switching is initiated in B cells.…”

Section: Escape From Alcatraz: Evidence For Selective Stabilization Amentioning

confidence: 99%

Centromeres: The wild west of the post-genomic age

Zeitlin¹

2010

Epigenetics

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Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome

Cited by 80 publications

References 115 publications

Diversity in Requirement of Genetic and Epigenetic Factors for Centromere Function in Fungi

Diversity in Requirement of Genetic and Epigenetic Factors for Centromere Function in Fungi

Centromere repositioning in mammals

Centromeres: The wild west of the post-genomic age

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