Key divisions and cell specification during embryo pattern formation require SMU1-mediated splicing of CAK genes in...

Embryonic pattern formation and cell specification require precise cell division and cell cycle regulation. Splicing factors and the splicing of precursor mRNA (pre-mRNA) play significant roles in embryo development. However, how splicing factors control embryonic patterning via RNA splicing remains unclear. Here, we show that the mutation of SUPPRESSORS OF MEC-8 AND UNC-52 1 (SMU1), a conserved subunit of the spliceosomal B complex, causes compromised cell fate of the hypophysis and quiescent center (QC), failed embryonic root apical meristem (RAM) formation, as evidenced by altered WUSCHEL-RELATED HOMEOBOX 5 (WOX5) expression and perturbed auxin signaling. This results in smu1 embryo lethality. The splicing efficiency of three out of four CYCLIN-DEPENDENT KINASE ACTIVATOR (CAK) genes is decreased, leading to reduced protein levels in smu1 embryos. These CAK genes are required for hypophysis specification and embryonic RAM formation. SMU1 binds CAK transcripts in vitro and in vivo. Restoring the expression of either CAK gene partially rescues the defects in smu1 embryos, leading to the formation of QC-like cells, continued embryo development, and even the production of viable seeds. Our data suggest that SMU1 binds to CAK transcripts and promotes their splicing, enabling cell cycle progression to promote embryonic RAM formation.