Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function

Centromeres are essential genetic elements that enable spindle microtubule attachment for chromosome segregation during mitosis and meiosis. While this function is preserved across species, centromeres display an array of dynamic features, including: (1) rapidly evolving DNA; (2) wide evolutionary d...

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Main Authors: Elisa Balzano, Simona Giunta
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/11/8/912
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author Elisa Balzano
Simona Giunta
author_facet Elisa Balzano
Simona Giunta
author_sort Elisa Balzano
collection DOAJ
description Centromeres are essential genetic elements that enable spindle microtubule attachment for chromosome segregation during mitosis and meiosis. While this function is preserved across species, centromeres display an array of dynamic features, including: (1) rapidly evolving DNA; (2) wide evolutionary diversity in size, shape and organization; (3) evidence of mutational processes to generate homogenized repetitive arrays that characterize centromeres in several species; (4) tolerance to changes in position, as in the case of neocentromeres; and (5) intrinsic fragility derived by sequence composition and secondary DNA structures. Centromere drive underlies rapid centromere DNA evolution due to the “selfish” pursuit to bias meiotic transmission and promote the propagation of stronger centromeres. Yet, the origins of other dynamic features of centromeres remain unclear. Here, we review our current understanding of centromere evolution and plasticity. We also detail the mutagenic processes proposed to shape the divergent genetic nature of centromeres. Changes to centromeres are not simply evolutionary relics, but ongoing shifts that on one side promote centromere flexibility, but on the other can undermine centromere integrity and function with potential pathological implications such as genome instability.
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spelling doaj.art-69b6f7c639c44974bed35ea0cc55ddc12023-11-20T09:38:37ZengMDPI AGGenes2073-44252020-08-0111891210.3390/genes11080912Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved FunctionElisa Balzano0Simona Giunta1Dipartimento di Biologia e Biotecnologie “Charles Darwin”, Sapienza Università di Roma, 00185 Roma, ItalyLaboratory of Chromosome and Cell Biology, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USACentromeres are essential genetic elements that enable spindle microtubule attachment for chromosome segregation during mitosis and meiosis. While this function is preserved across species, centromeres display an array of dynamic features, including: (1) rapidly evolving DNA; (2) wide evolutionary diversity in size, shape and organization; (3) evidence of mutational processes to generate homogenized repetitive arrays that characterize centromeres in several species; (4) tolerance to changes in position, as in the case of neocentromeres; and (5) intrinsic fragility derived by sequence composition and secondary DNA structures. Centromere drive underlies rapid centromere DNA evolution due to the “selfish” pursuit to bias meiotic transmission and promote the propagation of stronger centromeres. Yet, the origins of other dynamic features of centromeres remain unclear. Here, we review our current understanding of centromere evolution and plasticity. We also detail the mutagenic processes proposed to shape the divergent genetic nature of centromeres. Changes to centromeres are not simply evolutionary relics, but ongoing shifts that on one side promote centromere flexibility, but on the other can undermine centromere integrity and function with potential pathological implications such as genome instability.https://www.mdpi.com/2073-4425/11/8/912centromererepetitive DNAmutagenesiscentromere evolutionHORschromosome instability
spellingShingle Elisa Balzano
Simona Giunta
Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
Genes
centromere
repetitive DNA
mutagenesis
centromere evolution
HORs
chromosome instability
title Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
title_full Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
title_fullStr Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
title_full_unstemmed Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
title_short Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function
title_sort centromeres under pressure evolutionary innovation in conflict with conserved function
topic centromere
repetitive DNA
mutagenesis
centromere evolution
HORs
chromosome instability
url https://www.mdpi.com/2073-4425/11/8/912
work_keys_str_mv AT elisabalzano centromeresunderpressureevolutionaryinnovationinconflictwithconservedfunction
AT simonagiunta centromeresunderpressureevolutionaryinnovationinconflictwithconservedfunction