Adaptation of centromeres to breakage through local genomic and epigenomic remodeling in wheat

Abstract

Centromeres, characterized by their unique chromatin attributes, are indispensable for safeguarding genomic stability. Due to their intricate and fragile nature, centromeres are susceptible to chromosomal rearrangements. However, the mechanisms preserving their functional integrity and supporting nuclear homeostasis following breakages remain enigmatic. In this study, we use wheat ditelosomic stocks, which arise from centromere breakage, to explore the genetic and epigenetic alterations in damaged centromeres. Our investigations suggest novel chromosome end structures marked by de novo addition of telomeres, as well as localized chromosomal shattering, including segment deletions and duplications near centromere breakpoints. We reveal that the damaged centromeres possess a remarkable capacity for self-regulation, through employing structural modifications such as expansion, contraction, and neocentromere formation to maintain their functional integrity. Centromere breakage triggers nucleosome remodeling and is accompanied by local transcription changes and chromatin reorganization, and subsequently may contribute to the stabilization of broken chromosomes. Our findings highlight the resilience and adaptability of plant chromosomes in response to centromere breakage and provide valuable insights into the stability of centromeres, thereby offering promising prospects to manipulate centromeres for targeted chromosomal innovation and crop genetic improvement.