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.
Highlights
A sexual life cycle consisting of alternating haploid and diploid life forms is the defining feature of eukaryotes
We showed that Arabidopsis partially deficient in the RNA decay factor SUPPRESSOR WITH MORPHOGENETIC EFFECTS ON GENITALIA7 (SMG7) fail to exit meiosis and continue with attempts to undergo additional cycles of post-meiotic chromosome segregations without genome replication
Meiosis in smg7-6 pollen mother cells (PMCs) is followed by multiple rounds of spindle reassembly prior to polyad formation
Summary
A sexual life cycle consisting of alternating haploid and diploid life forms is the defining feature of eukaryotes. Entry into the haploid phase requires meiosis, a reductional cell division that forms four haploid cells from a single diploid precursor. It involves segregation of homologous chromosomes in the first meiotic division that is followed, without intervening DNA replication, by segregation of sister chromatids in the second meiotic division. In contrast to the mitotic cell division machinery, meiosis requires mechanisms for tethering homologous chromosomes via recombination in prophase I, sister kinetochore monoorientation and protection of centromeric cohesion in metaphase-anaphase I, and inhibition of DNA replication in interkinesis [1,2]. A number of genes involved in induction, progression, and termination of the meiotic program have been identified in plants. Entry into meiosis is further accompanied by the induction of genes required for core meiotic functions [13,14]
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