CEPR1 function across plant lineages: peptide hormone recognition by cereal crop orthologs and developmental roles in barley

Arabidopsis peptide hormones from the C-TERMINALLY ENCODED PEPTIDE (CEP) family and their receptor, CEP RECEPTOR1 (CEPR1), integrate growth and development with environmental cues. Since cereals display anatomical differences to dicots, it is unknown if CEPR1 functions similarly in monocots and dicots. We investigated cereal CEPR1 function by introducing putative barley, rice, or maize CEPR1 orthologs into an Arabidopsis cepr1 mutant to determine if its diverse root, vegetative development, and fecundity phenotypes could be restored. The monocot CEPR1 genes restored Arabidopsis root, shoot, seed phenotypes, and CEP DOWNSTREAM 1 expression. To validate cereal CEPR1 function, we knocked out CEPR1 in barley using CRISPR-Cas9. Barley cepr1 plants had steeper seminal roots, a narrower mature root system, and a severe fecundity defect, comparable to Atcepr1. As Atcepr1 complementation by barley CEPR1 necessitates interaction with native AtCEPs, we tested if Arabidopsis and barley CEPR1 favour interacting with CEPs from either species. AtCEPR1 favoured AtCEP3 due to divergence at the HvCEP N-terminus, whereas HvCEPR1 interacted with both Arabidopsis and barley CEPs. These results reveal CEP receptor function for cereal CEPR1s, developmental roles for barley CEPR1 in root architecture and fecundity, and imply that the CEPR1 pathway is a promising target for improving root architecture in cereals.