The Genetics and Epigenetics of Maize Centromeres
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2022
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Centromeres are chromosomal structures defined epigenetically by the histone cenH3. These structures are required for the faithful segregation of chromosomes during cell division, and survival of all eukaryotic organisms. The sequences of the centromere are highly repetitive, primarily containing tandem repeats and transposable elements. Remarkably, the repeats and proteins involved in centromere function evolve rapidly though the function of centromeres is highly conserved, a phenomenon referred to as the “centromere paradox”. This has been interpreted to be due to evolutionary pressure on both molecules based on their interaction (centromere drive). Recent investigations into domesticated maize have shown that artificial selection and genetic bottlenecks during domestication heavily influenced the evolution of domesticated centromeres, rather than the interplay of centromeric repeats and proteins as hypothesized by meiotic drive. Disruption of the ancestral centromere has the potential to cause the formation of a neocentromere in the pericentromere or chromosome arm. In Zea mays, loss of the centromeric tandem repeat centC has the potential to destabilize centromeres. When the centC is lost cenH3 can either spread into the chromatin flanking centC, or jump to a new locus entirely. Our investigations have determined that the jump from CEN5M to CEN5L or CEN5R was the result of transcribed genes flanking CEN5M which restricted the spread of cenH3 into flanking regions following loss of centC. The pericentromeres provide relatively ideal locations for neocentromere formation due to low transcription. The newly formed neocentromeres were stabilized through the loss of a H2A.Z loci that were shown to destabilize cenH3, via deletions and suppression by cenH3. Regions of limited recombination surrounding centromeres were defined by structural variation and selection in CEN2 and it was observed that a tight linkage between a domestication locus to a centromeric haplotype region can reduce the observed centromeric diversity likely due to linkage drag. Following the formation of neocentromeres they were rapidly colonized by CR2 retrotransposons which expanded in a burst event during domestication. There was extensive recombination among these elements, but a preferred recombination was not responsible for their expansion. It is possible that expansion of the CR2 subfamily was the result of horizontal transfer of a foreign CR2 element, or the result of epigenetic changes in the ancestral centromere following neocentromere formation. Regardless of the trigger for expansion, the CR2 insertions served to further stabilize the neocentromeres by increasing the repeat content and pushing sensitive DNA such as genes and regulatory regions out of the neocentromeres. Overall, these investigations suggest the story of domesticated maize centromere evolution was one of stability. The process of domestication destabilized the centromeres, and the centromeres have since been evolving to reacquire stability in a new genomic context.
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Bioinformatics, Agriculture, Genetics
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236 pages
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