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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-mediate genome elimination. Author summary: Meiosis is a reductional cell division that halves number of chromosomes during two successive rounds of chromosome segregation without intervening DNA replication. Such mode of chromosome segregation requires extensive reprogramming of the cell division machinery at the entry to meiosis, and inactivation of the meiotic program upon the formation of haploid spores. Here we showed that Arabidopsis partially deficient in the RNA decay factor SMG7 fail to exit meiosis and continue with attempts to undergo additional cycles of post-meiotic chromosome segregations without genome replication. This results in a reduced number of viable pollen and diminished fertility. To find genes involved in meiotic exit, we performed a suppressor screen for the SMG7-deicient plants that re-gain fertility. We found that reducing the amount of centromeric histone partially restores pollen formation and fertility in smg7 mutants. This is likely due to inefficient formation of centromere-microtubule interactions that impairs spindle reassembly and re-entry into aberrant rounds of post-meiotic chromosome segregation. [ABSTRACT FROM AUTHOR]