title: Two-ligand priming mechanism for potentiated phosphoinositide synthesis is an evolutionarily conserved feature of Sec14-like phosphatidylinositol and phosphatidylcholine exchange proteins.
abstract: Lipid signaling, particularly phosphoinositide signaling, plays a key role in regulating the extreme polarized membrane growth that drives root hair development in plants. The Arabidopsis AtSFH1 gene encodes a two-domain protein with an amino-terminal Sec14-like phosphatidylinositol transfer protein (PITP) domain linked to a carboxy-terminal nodulin domain. AtSfh1 is critical for promoting the spatially highly organized phosphatidylinositol-4,5-bisphosphate signaling program required for establishment and maintenance of polarized root hair growth. Here we demonstrate that, like the yeast Sec14, the AtSfh1 PITP domain requires both its phosphatidylinositol (PtdIns)- and phosphatidylcholine (PtdCho)-binding properties to stimulate PtdIns-4-phosphate [PtdIns(4)P] synthesis. Moreover, we show that both phospholipid-binding activities are essential for AtSfh1 activity in supporting polarized root hair growth. Finally, we report genetic and biochemical evidence that the two-ligand mechanism for potentiation of PtdIns 4-OH kinase activity is a broadly conserved feature of plant Sec14-nodulin proteins, and that this strategy appeared only late in plant evolution. Taken together, the data indicate that the PtdIns/PtdCho-exchange mechanism for stimulated PtdIns(4)P synthesis either arose independently during evolution in yeast and in higher plants, or a suitable genetic module was introduced to higher plants from a fungal source and subsequently exploited by them.
authors.affiliation: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, College Station, TX 77843-1114.
authors.forename: Jin
authors.initials: J
authors.lastname: Huang
authors.affiliation: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, College Station, TX 77843-1114.
authors.forename: Ratna
authors.initials: R
authors.lastname: Ghosh
authors.affiliation: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, College Station, TX 77843-1114.
authors.forename: Ashutosh
authors.initials: A
authors.lastname: Tripathi
authors.affiliation: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, College Station, TX 77843-1114.
authors.forename: Max
authors.initials: M
authors.lastname: Lönnfors
authors.affiliation: Faculty of Medicine, Department of Biochemistry and Developmental Biology, University of Helsinki, 00290 Helsinki, Finland.
authors.forename: Pentti
authors.initials: P
authors.lastname: Somerharju
authors.affiliation: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, College Station, TX 77843-1114 Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128 Department of Chemistry, Texas A&M University, College Station, TX 77840 vytas@tamhsc.edu.
authors.forename: Vytas A
authors.initials: VA
authors.lastname: Bankaitis
mesh_terms: D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000378:metabolism*; D008024:Ligands; D008565:Membrane Proteins / Q000378:metabolism; D010713:Phosphatidylcholines / Q000378:metabolism; D018129:Phosphatidylinositol Phosphates / Q000378:metabolism; D010716:Phosphatidylinositols / Q000096:biosynthesis* / Q000378:metabolism; D049294:Phospholipid Transfer Proteins / Q000378:metabolism*; D010940:Plant Proteins / Q000378:metabolism; D018517:Plant Roots / Q000378:metabolism; D011485:Protein Binding; D000072417:Protein Domains; D015398:Signal Transduction
chemical_list: D029681:Arabidopsis Proteins; D008024:Ligands; D008565:Membrane Proteins; D010713:Phosphatidylcholines; D018129:Phosphatidylinositol Phosphates; D010716:Phosphatidylinositols; D049294:Phospholipid Transfer Proteins; D010940:Plant Proteins; C000606246:Sfh1 protein, Arabidopsis; C045625:nodulin