A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis

PLoS Genet. 2021 Sep 30;17(9):e1009779. doi: 10.1371/journal.pgen.1009779. eCollection 2021 Sep.

Abstract

Meiosis in angiosperm plants is followed by mitotic divisions to form multicellular haploid gametophytes. Termination of meiosis and transition to gametophytic development is, in Arabidopsis, governed by a dedicated mechanism that involves SMG7 and TDM1 proteins. Mutants carrying the smg7-6 allele are semi-fertile due to reduced pollen production. We found that instead of forming tetrads, smg7-6 pollen mother cells undergo multiple rounds of chromosome condensation and spindle assembly at the end of meiosis, resembling aberrant attempts to undergo additional meiotic divisions. A suppressor screen uncovered a mutation in centromeric histone H3 (CENH3) that increased fertility and promoted meiotic exit in smg7-6 plants. The mutation led to inefficient splicing of the CENH3 mRNA and a substantial decrease of CENH3, resulting in smaller centromeres. The reduced level of CENH3 delayed formation of the mitotic spindle but did not have an apparent effect on plant growth and development. We suggest that impaired spindle re-assembly at the end of meiosis limits aberrant divisions in smg7-6 plants and promotes formation of tetrads and viable pollen. Furthermore, the mutant with reduced level of CENH3 was very inefficient haploid inducer indicating that differences in centromere size is not the key determinant of centromere-mediated genome elimination.

Grant support

This work was supported from the European Regional Development Fund‐Project ‘REMAP’ (No. CZ.02.1.01/0.0/0.0/15_003/0000479 to K.R.), Doctoral School “Chromosome Dynamics” of the Austrian Science Fund (FWF W1238 to K.R. and O.M.S.), Vienna Science and Technology Fund (WWTF LS13-057 to O.M.S.) and the German Federal Ministry of Education and Research (Plant 2030, Project 031B0192NN, HaploTools, to I.L.). The core facility CELLIM of CEITEC is supported by MEYS CR (LM2018129 Czech-BioImaging). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Funders web sites: MEYS: https://www.msmt.cz/ Austrian Science Fund: https://www.fwf.ac.at/ Vienna Science and Technology Fund: https://www.wwtf.at/ German Federal Ministry of Education and Research https://www.bmbf.de/.