Widespread Gene Conversion in Centromere Cores
Open Access
- 9 March 2010
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Biology
- Vol. 8 (3), e1000327
- https://doi.org/10.1371/journal.pbio.1000327
Abstract
Centromeres are the most dynamic regions of the genome, yet they are typified by little or no crossing over, making it difficult to explain the origin of this diversity. To address this question, we developed a novel CENH3 ChIP display method that maps kinetochore footprints over transposon-rich areas of centromere cores. A high level of polymorphism made it possible to map a total of 238 within-centromere markers using maize recombinant inbred lines. Over half of the markers were shown to interact directly with kinetochores (CENH3) by chromatin immunoprecipitation. Although classical crossing over is fully suppressed across CENH3 domains, two gene conversion events (i.e., non-crossover marker exchanges) were identified in a mapping population. A population genetic analysis of 53 diverse inbreds suggests that historical gene conversion is widespread in maize centromeres, occurring at a rate >1×10−5/marker/generation. We conclude that gene conversion accelerates centromere evolution by facilitating sequence exchange among chromosomes. Centromeres, which harbor the attachment points for microtubules during cell division, are characterized by repetitive DNA, paucity of genes, and almost complete suppression of crossing over. The repetitive DNA within centromeres appears to evolve much faster than would be expected for genetically inert regions, however. Current explanations for this rapid evolution tend to be theoretical. On the one hand there are arguments that subtle forms of selection on selfish repeat sequences can explain the rapid rate of change, while on the other hand it seems plausible that some form of accelerated neutral evolution is occurring. Here, we address this question in maize, which is known for its excellent genetic mapping resources. We first developed a method for identifying hundreds of single copy markers in centromeres and confirmed that they lie within functional domains by using a chromatin immunoprecipitation assay for kinetochore protein CENH3. All markers were mapped in relation to each other. The data show that, whereas classical crossing over is suppressed, there is extensive genetic exchange in the form of gene conversion (by which short segments of one chromosome are copied onto the other). These results were confirmed by demonstrating that similar short exchange tracts are common among the centromeres from multiple diverse inbred lines of maize. Our study suggests that centromere diversity can be at least partially attributed to a high rate of previously “hidden” genetic exchange within the core kinetochore domains.Keywords
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