CCCH-type zinc finger proteins are required for meiotic progression and RNA clearance in Arabidopsis

In animals and plants, the zygotene to pachytene transition of male meiocytes is marked by programmed mRNA degradation. In animals this is essential for meiotic progression, but in plants its role and underlying mechanism remain unknown. Here, we identify the tandem CCCH-type zinc finger proteins C3H14 and C3H15 as central regulators of RNA degradation in the microspore mother cells (MMCs) of Arabidopsis (Arabidopsis thaliana). We show that C3H14/15 are expressed at high levels in MMCs during the zygotene to pachytene transition, where they bind highly expressed mRNAs, including many that encode ribosomal, mitochondrial, and plastid proteins. Loss of C3H14/15 results in the formation of excess DNA:RNA hybrids, genomic instability, failure to progress beyond the pachytene stage of meiosis, and finally DNA degradation and cell death. Moreover, we show that C3H15 accumulates in P-bodies through its interaction with the decapping enzyme DCP1 for RNA degradation. Our findings establish mRNA decay mediated by C3H14/15 as a critical regulatory mechanism safeguarding meiosis in plants, highlighting the convergence of RNA metabolism and genome stability pathways during a key developmental transition.