Epigenetically mismatched parental centromeres trigger genome elimination in hybrids.

Mohan P A Marimuthu,Luca Comai,Ravi Maruthachalam,Anne Britt,Sundaram Kuppu,Ek Han Tan,Simon W L Chan,Ramesh Bondada

doi:10.1126/sciadv.abk1151

Abstract

Wide crosses result in postzygotic elimination of one parental chromosome set, but the mechanisms that result in such differential fate are poorly understood. Here, we show that alterations of centromeric histone H3 (CENH3) lead to its selective removal from centromeres of mature Arabidopsis eggs and early zygotes, while wild-type CENH3 persists. In the hybrid zygotes and embryos, CENH3 and essential centromere proteins load preferentially on the CENH3-rich centromeres of the wild-type parent, while CENH3-depleted centromeres fail to reconstitute new CENH3-chromatin and the kinetochore and are frequently lost. Genome elimination is opposed by E3 ubiquitin ligase VIM1. We propose a model based on cooperative binding of CENH3 to chromatin to explain the differential CENH3 loading rates. Thus, parental CENH3 polymorphisms result in epigenetically distinct centromeres that instantiate a strong mating barrier and produce haploids.

Highlights

Uniparental genome elimination (GE) entails the postzygotic loss of one parental chromosome set
Among the haploid inducer (HI) (Fig. 1A), the green fluorescent protein-tailswap (GFP-ts) variant is highly efficient in triggering GE when crossed to WT male (Fig. 1B)
Lines coexpressing endogenous centromeric histone H3 (CENH3) and GFP-ts behave as wild type [2], yielding only diploid progeny on crossing to wild-type male and were used as an isogenic control cross (CC) (Fig. 1D)

Summary

Introduction

Uniparental genome elimination (GE) entails the postzygotic loss of one parental chromosome set. Distant hybridization can result in GE [1], but notwithstanding their basic scientific interest and their usefulness in producing haploids for breeding, little is known about what mechanisms mediate identification and selective missegregation of one parental chromosome set. When a cenh embryo-lethal mutant in Arabidopsis is complemented by a haploid inducer (HI) CENH3 variant (Fig. 1A), selfing has no effect on seed set or genome maintenance [2, 6,7,8], but outcrossing to the wild-type (WT) male results in ~70% seed death. CENH3 and the kinetochore assemble on the CENH3rich centromeres inherited from the wild-type parent, but not on those from the HI. We propose a model to explain the differential CENH3 loading rates by a cooperative binding effect

Methods

Results

Conclusion