Zinc-finger proteins C3H14 and C3H15 maintain meiocyte identity in flowering plants

In the anthers of flowering plants, the innermost meiocytes and surrounding somatic cells (tapetum) are differentiated from the same precursor archesporial cells, and these cells acquire distinct cell identities after specification. However, the underlying mechanism regulating meiocyte identity is elusive. Here we demonstrate a conserved surveillance mechanism governed by Arabidopsis zinc-finger proteins C3H14 and C3H15, which redundantly regulate mRNA homoeostasis to ensure meiocyte identity. The meiocytes of Atc3h14 Atc3h15 display meiotic arrest accompanied by ectopic accumulation of mRNAs essential for archesporial cell differentiation and tapetum development. These meiocytes ultimately undergo reactive oxygen species bursts and programmed cell death in synchrony with the tapetum. Moreover, C3H14/C3H15 interacts with processing-body proteins and the CCR4-NOT deadenylase complex, and is required for eliminating unwanted transcripts. Consistently, CRISPR-Cas9-induced mutations in AtC3H14/15 paralogues in soybean and rice caused similar defects in meiocyte identity, indicating that the regulation of meiocyte identity by post-transcriptional RNA elimination is conserved in flowering plants.