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Curr Biol 2022 Sep 26;3218:3939-3951.e6. doi: 10.1016/j.cub.2022.07.037.
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Molecular conflicts disrupting centromere maintenance contribute to Xenopus hybrid inviability.

Kitaoka M , Smith OK , Straight AF , Heald R .

Although central to evolution, the causes of hybrid inviability that drive reproductive isolation are poorly understood. Embryonic lethality occurs when the eggs of the frog X. tropicalis are fertilized with either X. laevis or X. borealis sperm. We observed that distinct subsets of paternal chromosomes failed to assemble functional centromeres, causing their mis-segregation during embryonic cell divisions. Core centromere DNA sequence analysis revealed little conservation among the three species, indicating that epigenetic mechanisms that normally operate to maintain centromere integrity are disrupted on specific paternal chromosomes in hybrids. In vitro reactions combining X. tropicalis egg extract with either X. laevis or X. borealis sperm chromosomes revealed that paternally matched or overexpressed centromeric histone CENP-A and its chaperone HJURP could rescue centromere assembly on affected chromosomes in interphase nuclei. However, although the X. laevis chromosomes maintained centromeric CENP-A in metaphase, X. borealis chromosomes did not and also displayed ultra-thin regions containing ribosomal DNA. Both centromere assembly and morphology of X. borealis mitotic chromosomes could be rescued by inhibiting RNA polymerase I or preventing the collapse of stalled DNA replication forks. These results indicate that specific paternal centromeres are inactivated in hybrids due to the disruption of associated chromatin regions that interfere with CENP-A incorporation, at least in some cases due to conflicts between replication and transcription machineries. Thus, our findings highlight the dynamic nature of centromere maintenance and its susceptibility to disruption in vertebrate interspecies hybrids.

PubMed ID: 35973429
PMC ID: PMC9529917
Article link: Curr Biol
Grant support: [+]

Species referenced: Xenopus tropicalis Xenopus laevis Xenopus borealis
Genes referenced: aurka blmh eif4g2 plk1 ubtf
GO keywords: chromosome [+]
Antibodies: H3f3a Ab33 Myc Ab2

Article Images: [+] show captions
References [+] :
Anselm, Oligomerization of Drosophila Nucleoplasmin-Like Protein is required for its centromere localization. 2019, Pubmed