The PP2CH- and PBL27-mediated phosphorylation switch of aluminium ion receptor PSKR1/ALR1 controls plant aluminum sensing ability.

The ability of plants to sense toxic and nutrient ions is critical for their growth and survival, yet how this ability is regulated remains largely unknown. We previously identified the receptor-like kinase PSKR1/ALR1 (ALR1) in Arabidopsis as a receptor that senses phytotoxic aluminium (Al) ions, which cause severe crop yield loss and forest decline on acidic soils widely distributed over the world. Here we further show that the phosphorylation status of specific Ser residues in ALR1(Ser696/698) controls plant Al-sensing ability. ALR1(Ser696/698) phosphorylation levels are rapidly reduced by Al ions, and the dephosphorylation promotes the interaction and inter-phosphorylation of ALR1 and the BAK1 coreceptor, thereby activating STOP1-dependent Al signalling and resistance. We next identify a clade of PP2C-type phosphatases (PP2CH1 and PP2CH2) that mediate the dephosphorylation of ALR1(Ser696/698). We show that Al ions rapidly increase the protein accumulation of PP2CH1/2 and promote their interaction with ALR1. The lack of both PP2CHs notably increases the phosphorylation levels of ALR1(Ser696/698), therefore reducing the strength of Al signalling. Additionally, we found a receptor-like cytoplasmic kinase, PBL27, responsible for phosphorylating ALR1(Ser696/698) and playing a negative role in the regulation of ALR1-mediated Al signalling. These findings uncover a phosphatase/kinase-mediated phosphorylation switching mechanism of ALR1 that controls plant Al-sensing ability, providing insights into ion-sensing mechanisms in living organisms.