Higher order repeat structures reflect diverging evolutionary paths in maize centromeres and knobs

Abstract

BackgroundHighly repetitive tandem repeat arrays, known as satellite DNAs, are enriched in low-recombination regions such as centromeres. Satellite arrays often contain complex internal structures called higher-order repeats (HORs), which may have functional significance. Maize is unusual in that its satellites occur in two distinct genomic contexts: centromeres, which interact with kinetochore proteins, and knobs, which undergo meiotic drive in the presence of Abnormal chromosome 10. Whether maize centromeres or knobs contain HOR patterns, and how such patterns relate to function, remains unclear. ResultsHere, we generate 13 repeat-sensitive genome assemblies of maize and its recent ancestor, teosinte. We develop a new graph-based pipeline, HiReNET, to classify HORs and demonstrate its utility in both Arabidopsis and maize. We find that HORs are ubiquitous in maize satellites but are typically low-frequency with small patterns, unlike the large, continuous HOR blocks characteristic of human centromeres. Approximately 38% of centromeric CentC monomers occur in HORs; however, no specific HOR class dominates any functional centromere as marked by centromeric histone H3. Arabidopsis centromeres have a similar HOR landscape. In contrast, maize knobs exhibit a more structured HOR distribution. Large knobs contain megabase-scale similarity blocks with repeated HOR patterns. These repeat units likely promote unequal crossing over, enabling rapid knob expansion, and may harbor motifs recognized by trans-acting factors involved in meiotic drive. ConclusionsHORs occur in all major maize satellite arrays. Specific HORs are not associated with centromere function, but knobs contain conserved HOR patterns within similarity blocks that may facilitate meiotic drive.