SUPPRESSOR OF MAX2 1-LIKE (SMXL) homologs are MAX2-dependent repressors of Physcomitrium patens growth

• Published in: The Plant cell 2024-05, Vol.36 (5), p.1655-1672
• Main Authors: Guillory, Ambre, Lopez-Obando, Mauricio, Bouchenine, Khalissa, Le Bris, Philippe, Lécureuil, Alain, Pillot, Jean-Paul, Steinmetz, Vincent, Boyer, François-Didier, Rameau, Catherine, de Saint Germain, Alexandre, Bonhomme, Sandrine
• Format: Article
• Language: English
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1093/plcell/koae009

Abstract SUPPRESSOR OF MAX2 (SMAX)1-LIKE (SMXL) proteins are a plant-specific clade of type I HSP100/Clp-ATPases. SMXL genes are present in virtually all land plant genomes. However, they have mainly been studied in angiosperms. In Arabidopsis (Arabidopsis thaliana), 3 functional SMXL subclades have been identified: SMAX1/SMXL2, SMXL345, and SMXL678. Of these, 2 subclades ensure endogenous phytohormone signal transduction. SMAX1/SMXL2 proteins are involved in KAI2 ligand (KL) signaling, while SMXL678 proteins are involved in strigolactone (SL) signaling. Many questions remain regarding the mode of action of these proteins, as well as their ancestral roles. We addressed these questions by investigating the functions of the 4 SMXL genes in the moss Physcomitrium patens. We demonstrate that PpSMXL proteins are involved in the conserved ancestral MAX2-dependent KL signaling pathway and negatively regulate growth. However, PpSMXL proteins expressed in Arabidopsis cannot replace SMAX1 or SMXL2 function in KL signaling, whereas they can functionally replace SMXL4 and SMXL5 and restore root growth. Therefore, the molecular functions of SMXL proteins are conserved, but their interaction networks are not. Moreover, the PpSMXLC/D clade positively regulates SL signal transduction in P. patens. Overall, our data reveal that SMXL proteins in moss mediate crosstalk between the SL and KL signaling pathways. SMXL proteins repress Physcomitrium patens growth through a conserved ancestral signaling pathway.