Only the Rye Derived Part of the 1BL/1RS Hybrid Centromere Incorporates CENH3 of Wheat

Abstract

The precise assembly of the kinetochore complex at the centromere is epigenetically determined by substituting histone H3 with the centromere-specific histone H3 variant CENH3 in centromeric nucleosomes. The wheat-rye 1BL/1RS translocation chromosome in the background of wheat resulted from a centric misdivision followed by the fusion of the broken arms of chromosomes 1B and 1R from wheat and rye, respectively. The resulting hybrid (dicentric)centromere is composed of both wheat and rye centromeric repeats. As CENH3 is a marker for centromere activity, we applied Immuno-FISH followed by ultrastructural super-resolution microscopy to address whether both or only parts of the hybrid centromere are active. Our study demonstrates that only the rye-derived centromere part incorporates CENH3 of wheat in the 1BL/1RS hybrid centromere. This finding supports the notion that one centromere part of a translocated chromosome undergoes inactivation, creating functional monocentric chromosomes to maintain chromosome stability.

Young retrotransposons and non‐B DNA structures promote the establishment of dominant rye centromere in the 1RS.1BL fused centromere

“…Moreover, none of the CENH3 variants from rye are encoded by the short arm of chromosome 1R in 1RS.1BL translocations. Consequently, the CENH3 located on 1RS.1BL is of wheat origin (Wang et al ., 2017; Karimi‐Ashtiyani et al ., 2021). We hypothesized that after the formation of CS.1RS/1BL translocation line, the CENH3 nucleosome positioning or CENH3‐binding domains on rye centromeric repeats may underwent adaptation process to determine centromere identity.…”

“…To maintain chromosome stability, one of the centromeres in a translocated chromosome undergoes inactivation. This process creates a functional monocentric chromosome, which means that the chromosome has only one active centromere (Karimi‐Ashtiyani et al ., 2021). Differential selection appears to operate between the rye 1RS and wheat 1BL centromeres for the binding of active CENH3.…”

“…The precise positioning of CENH3 nucleosomes is epigenetically preserved within the centromeric repeats among wheat 10+ lines (Ma et al, 2023). Therefore, the centromere sequence from the difference rye accession employed in the generation of the (Wang et al, 2017;Karimi-Ashtiyani et al, 2021). We hypothesized that after the formation of CS.1RS/ 1BL translocation line, the CENH3 nucleosome positioning or CENH3-binding domains on rye centromeric repeats may underwent adaptation process to determine centromere identity.…”

Permanent Spreading of 1RS.1AL and 1RS.1BL Translocations in Modern Wheat Breeding

“…Revealed 1RS.1BL and 1RS.1AL rearrangements are typical centric breakage-fusion chromosomes demonstrating stable mitotic stable chromosomes capable of normal behavior in cell divisions in common wheat [ 54 ]. Apparently, the stability of 1RS.1BL is due to the fact that the wheat centromere is inactivated and only the rye-derived centromere part incorporates CENH3, since centromeres with several active centromere units may have increased fragility and may result in new breakage and telocentric formation [ 55 , 56 ]. Thus, the centric type of 1RS chromosomal rearrangement remains the most common among commercial varieties.…”

Molecular and Cytogenetic Identification of Wheat-Thinopyrum intermedium Double Substitution Line-Derived Progenies for Stripe Rust Resistance

“…It is likely that centromere-associated DNA sequences are not fixed but are dynamic in their amounts and positions on chromosomes in Triticeae. Further studies will be performed to reveal the Thinopyrum -derived centromere incorporated CENH3 of wheat in the wheat-1St or wheat-4J S L hybrid centromere, as well as the mechanism of wheat- Thinopyrum translocated chromosomes for maintaining their chromosome stability with respect to evolutionary and breeding purposes [ 44 , 45 ].…”