A SAC Phosphoinositide Phosphatase Controls Rice Development via Hydrolyzing PI4P and PI(4,5)P2

Phosphoinositides (PIs) as regulatory membrane lipids play essential roles in multiple cellular processes. Although the exact molecular targets of PI-dependent modulation remain largely elusive, the effects of disturbed PI metabolism could be employed to identify regulatory modules associated with particular downstream targets of PIs. Here, we identified the role of GRAIN NUMBER AND PLANT HEIGHT1 ( GH1 ), which encodes a suppressor of actin (SAC) domain-containing phosphatase with unknown function in rice ( Oryza sativa ). Endoplasmic reticulum-localized GH1 specifically dephosphorylated and hydrolyzed phosphatidylinositol 4-phosphate (PI4P) and phosphatidylinositol 4,5-bisphosphate [PI(4,5)P 2 ]. Inactivation of GH1 resulted in massive accumulation of both PI4P and PI(4,5)P 2 , while excessive GH1 caused their depletion. Notably, superabundant PI4P and PI(4,5)P 2 could both disrupt actin cytoskeleton organization and suppress cell elongation. Interestingly, both PI4P and PI(4,5)P 2 inhibited actin-related protein2 and -3 (Arp2/3) complex-nucleated actin-branching networks in vitro, whereas PI(4,5)P 2 showed more dramatic effects in a dose-dependent manner. Overall, the overaccumulation of PI(4,5)P 2 resulting from dysfunction of SAC phosphatase possibly perturbs Arp2/3 complex-mediated actin polymerization, thereby disordering cell development. These findings imply that the Arp2/3 complex might be the potential molecular target of PI(4,5)P 2 -dependent modulation in eukaryotes, thereby providing insights into the relationship between PI homeostasis and plant growth and development.