Physcomitrium patensSMXL homologs are PpMAX2-dependent negative regulators of growth

SMXL proteins are a plant-specific clade of type I HSP100/Clp-ATPases.SMXLgenes are found in virtually all land plants’ genomes. However, they have mainly been studied in angiosperms. InArabidopsis thaliana, three SMXL functional subclades have been identified: SMAX1/SMXL2, SMXL345 and SMXL678. Out of these, two subclades ensure transduction on endogenous hormone signals: SMAX1/SMXL2 are involved in KAI2-ligand (KL) signaling, while SMXL678 are involved in strigolactones (SLs) signaling. Many questions remain regarding the mode of action of these proteins, as well as their ancestral role. In light of recent discoveries in the liverwortMarchantia polymorpha,we addressed this second question by investigating the function of the fourSMXLgenes of the mossPhyscomitrium patens.We demonstrate that PpSMXL proteins are negative regulators of growth, involved in the likely conserved ancestral MAX2-dependent KL signaling pathway. However, PpSMXL proteins expressed inArabidopsis thalianaunexpectedly cannot replace SMAX1/SMXL2 function in KL signaling, whereas they can functionally replace SMXL4/5 and restore root growth. Therefore, the molecular function of SMXL could be conserved, but not their interaction network. Moreover, one PpSMXL clade also positively regulates transduction of the SL signal inP. patens, this function most probably having an independent evolutionary origin to angiosperms SMXL678.