Control of stem cell behavior by CLE-JINGASA signaling in the shoot apical meristem in Marchantia polymorpha

Land plants undergo indeterminate growth by the activity of meristems in both gametophyte (haploid) and sporophyte (diploid) generations1-3. In the sporophyte of the flowering plant Arabidopsis thaliana, the apical meristems are located at the shoot and root tips, in which a number of regulatory gene homologs are shared for their development, implying deep evolutionary origins4-7. However, little is known about their functional conservation with gametophytic meristems in distantly related land plants such as bryophytes8-17, even though genomic studies have revealed the subfamily-level diversity of regulatory genes is mostly conserved throughout land plants18-23. Here we show that a NAM/ATAF/CUC (NAC) domain transcription factor, JINGASA (MpJIN), acts downstream of CLV3/ESR-related (CLE) peptide signaling and controls stem cell behavior in the gametophytic shoot apical meristem of the liverwort Marchantia polymorpha. We found that MpJIN shows heterogeneous expression in space and time within the stem cell zone, associated with the loss and de novo specification of stem cell identity at the branching event. Consistent with the expression pattern, induction of MpJIN results in ectopic periclinal cell division in the stem cell zone and meristem termination. Comparative expression analysis suggests that the function of JIN/FEZ subfamily genes was shared between the shoot apical meristems in the gametophyte and sporophyte generations in early land plants but was lost in certain lineages including the flowering plant A. thaliana.