Arabidopsis PROTODERMAL FACTOR2 binds lysophosphatidylcholines and transcriptionally regulates phospholipid metabolism

Abstract

Plant homeodomain leucine-zipper IV (HD-Zip IV) transcription factors (TFs) contain an evolutionarily conserved steroidogenic acute regulatory protein (StAR)-related lipid transfer (START) domain. The START domain is required for TF activity; however, its presumed role as a lipid sensor is not well understood. Here we used tandem affinity purification from Arabidopsis cell cultures to demonstrate that PROTODERMAL FACTOR2 (PDF2), a representative family member which controls epidermal differentiation, recruits lysophosphatidylcholines in a START-dependent manner. In vitro assays with recombinant protein verified that a missense mutation in a predicted ligand contact site reduces lysophospholipid binding. We additionally uncovered that PDF2 controls the expression of phospholipid-related target genes by binding to a palindromic octamer with consensus to a phosphate (Pi) response element. Phospholipid homeostasis and elongation growth were altered in pdf2 mutants according to Pi availability. Cycloheximide chase experiments further revealed a role for START in maintaining protein levels, and Pi limitation resulted in enhanced protein destabilization, suggesting a mechanism by which lipid binding controls TF activity. We propose that the START domain serves as a molecular sensor for membrane phospholipid status in the epidermis. Overall our data provide insights towards understanding how the lipid metabolome integrates Pi availability with gene expression.