A plant CLE peptide and its fungal mimic promote arbuscular mycorrhizal symbiosis via CRN-mediated ROS suppression.

Abstract

CLAVATA3/EMBRYO SURROUNDING REGION-related (CLE) peptides have emerged as key regulators of plant-microbe interactions, including arbuscular mycorrhizal (AM) symbiosis. Here, we identify <i>Medicago truncatula</i> CLE16 as a positive regulator of AM symbiosis. <i>MtCLE16</i> is expressed in root cells colonized by AM fungi (AMF) and its overexpression within colonized tissues increases arbuscule abundance by finetuning their growth and lifespan. Functional and transcriptomic analyses reveal that MtCLE16 acts via the <i>M. truncatula</i> pseudokinase CORYNE (MtCRN) and suppresses the accumulation of reactive oxygen species (ROS) in roots, thereby attenuating immune responses and promoting root colonization by mutualistic AM fungi. Notably, AMF also express MtCLE16-like peptides. We show that the <i>Rhizophagus irregularis</i> MtCLE16-like peptide, RiCLE1, also attenuates ROS and promotes AMF colonization via MtCRN. This finding suggests that RiCLE1 can interfere with the MtCLE16-MtCRN signaling module of host roots to benefit the fungus. Our research uncovers a functional mechanism underpinning cross-kingdom signaling and molecular mimicry in mutualistic plant-microbe interactions.