Germline cell identity maintenance by a pair of zinc finger proteins C3H14 and C3H15 in flowering plants
In the anther of flowering plants, innermost germline cells (meiocytes) and surrounding somatic cells (tapetum) are differentiated from the same precursor archesporial cells (ARs), and these cells after specification acquire distinct cell identities. However, the maintenance of meiocyte identity is elusive. Here we demonstrate a conserved surveillance mechanism governed by Arabidopsis zinc-finger proteins C3H14 and C3H15, which regulate mRNA homeostasis to safeguard the meiocyte identity. C3H14/C3H15 interacts with P-body proteins and CCR4-NOT deadenylase complex, and is required for eliminating unwanted transcripts. Their deficiency induces ectopic accumulation of mRNAs essential for AR differentiation and tapetum development in meiocytes, thus resulting in a confused meiocyte identity with subsequently tapetum-like reactive oxygen species (ROS) bursts and programmed cell death (PCD). Furthermore, CRISPR-Cas9-induced mutations in AtC3H14/15 paralogs in soybean and rice caused similar defects in meiocyte identity maintenance, indicating that germline cell maintenance by post-transcriptional RNA elimination is conserved in flowering plants. Overall design: meiocytes from Arabidopsis col-0, c3h14, c3h15, and c3h14 c3h15 with two replicates; inflorescence meristem and anther at stage 2 from col-0 with three replicates; 21-day old leaves from col-0 and c3h14 c3h15 with three replicates.