E2fl1 is a meiosis-specific transcription factor in the protist <i>Tetrahymena thermophila</i>

Members of the E2F family of transcription factors have been reported to regulate the expression of genes involved in cell cycle control, DNA replication, and DNA repair in multicellular eukaryotes. Here, <i>E2FL1</i>, a meiosis-specific E2F transcription factor gene, was identified in the model ciliate <i>Tetrahymena thermophila</i>. Loss of this gene resulted in meiotic arrest prior to anaphase I. The cytological experiments revealed that the meiotic homologous pairing was not affected in the absence of <i>E2FL1</i>, but the paired homologous chromosomes did not separate and assumed a peculiar tandem arrangement. This is the first time that an E2F family member has been shown to regulate meiotic events. Moreover, BrdU incorporation showed that DSB processing during meiosis was abnormal upon the deletion of <i>E2FL1</i>. Transcriptome sequencing analysis revealed that <i>E2FL1</i> knockout decreased the expression of genes involved in DNA replication and DNA repair in <i>T. thermophila</i>, suggesting that the function of E2F is highly conserved in eukaryotes. In addition, <i>E2FL1</i> deletion inhibited the expression of related homologous chromosome segregation genes in <i>T. thermophila</i>. The result may explain the meiotic arrest phenotype at anaphase I. Finally, by searching for E2F DNA-binding motifs in the entire <i>T. thermophila</i> genome, we identified 714 genes containing at least one E2F DNA-binding motif; of these, 235 downregulated represent putative <i>E2FL1</i> target genes.