† Jingwei Zhou and Yuhong Huang contributed equally to this work

* Corresponding authors: Handong Su (Email: shandong@mail.hzau.edu.cn)

Centromeres have unique chromatin features that play an essential role in maintaining genomic stability. Although they are intrinsically repetitive and fragile hotspots for chromosomal rearrangements, little is known about how centromeres maintain their integrity and ensure the homeostasis of nucleus when they are breakage.

In this study, we investigated the genetics and epigenetics of damaged centromeres in stocks of wheat ditelocentrics lines from centromere misdivisions. We show novel chromosome end structures with de novo telomere addition and subtelomere deletions following centromere misdivisions in common wheat. Local complex chromosome rearrangements were observed with segment deletion and copy number expansion, suggesting BFB cycle occurred at centromere break site in wheat.

Furthermore, we found maintenance, expansion and contraction centromere regions with remodeling nucleosome distributions, but preserve strict CENH3 nucleosome positioning on complex centromeric repeats. We also found that de novo centromeres were formed when the original centromere were lost. Local transcription and chromatin reorganizations were substantially associated with damaged centromere following centromere breakage in wheat.

These findings suggest how structure and function integrity of centromere is preserved in response to centromere damage. Ultimately, these results finely resolved chromosome end structures, providing knowledge about the consequences regarding repair processes after centromere dysfunction misdivision, suggesting insights into evolution of complex chromosome end structures in nature.