Evolutionary dynamics of the pan-centromere architecture in oaks

Abstract

Centromeres ensure faithful chromosome segregation and genome stability, yet their DNA evolves rapidly, presenting a long-standing centromere paradox. Here we characterise the genomic and epigenomic architecture of >1,300 candidate centromeres from 111 high-quality Quercus (oak) genomes. We show that lineage-specific expansion of QuCEN146 satellite drives centromere turnover in oaks by displacing ancestral LTR-rich sequences into flanking regions, with genetic drift facilitating fixation of satellite-rich centromeres. Population-scale analyses in Q. serrata reveal extensive variation in satellite rich centromeres, generated by array expansion and contraction, strand-orientation shifts, and interspecific introgression. By contrast, LTR rich centromeres of Q. variabilis exhibit extremely low polymorphism and high collinearity across populations, sustained by suppressed local recombination, linked selection, and constrained LTR dynamics. We further demonstrate chromosome-independent evolutionary patterns for both satellite-rich and LTR-rich centromeres. Collectively, these findings demonstrate how evolutionary processes drive centromere turnover and shape contrasting centromeric sequence landscapes in forest trees.