Sec14-nodulin proteins and the patterning of phosphoinositide landmarks for developmental control of membrane morphogenesis.
Polarized membrane morphogenesis is a fundamental activity of eukaryotic cells. This process is essential for the biology of cells and tissues, and its execution demands exquisite temporal coordination of functionally diverse membrane signaling reactions with high spatial resolution. Moreover, mechanisms must exist to establish and preserve such organization in the face of randomizing forces that would diffuse it. Here we identify the conserved AtSfh1 Sec14-nodulin protein as a novel effector of phosphoinositide signaling in the extreme polarized membrane growth program exhibited by growing Arabidopsis root hairs. The data are consistent with Sec14-nodulin proteins controlling the lateral organization of phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) landmarks for polarized membrane morphogenesis in plants. This patterning activity requires both the PtdIns(4,5)P2 binding and homo-oligomerization activities of the AtSfh1 nodulin domain and is an essential aspect of the polarity signaling program in root hairs. Finally, the data suggest a general principle for how the phosphoinositide signaling landscape is physically bit mapped so that eukaryotic cells are able to convert a membrane surface into a high-definition lipid-signaling screen.
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843.
Ratna
R
Ghosh
Center for Plant Molecular Biology, Plant Physiology, Universität Tübingen, 72076 Tübingen, Germany.
Marília K F
MK
de Campos
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843.
Jin
J
Huang
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843.
Seong K
SK
Huh
Department of Physics, Tampere University of Technology, FI-33101 Tampere, Finland.
Adam
A
Orlowski
Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843.
Yuan
Y
Yang
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843.
Ashutosh
A
Tripathi
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843.
Aaron
A
Nile
Center for Plant Molecular Biology, Plant Physiology, Universität Tübingen, 72076 Tübingen, Germany.
Hsin-Chieh
HC
Lee
Zentrum für Datenverarbeitung, Universität Tübingen, 72074 Tübingen, Germany.
Marek
M
Dynowski
Center for Plant Molecular Biology, Plant Physiology, Universität Tübingen, 72076 Tübingen, Germany.
Helen
H
Schäfer
Department of Physics, Tampere University of Technology, FI-33101 Tampere, Finland.
Tomasz
T
Róg
Unidad de Biofísica (CSIC, UPV/EHU), Departamento de Bioquímica, Universidad del País Vasco, 48940 Leioa, Spain.
Marta G
MG
Lete
Unidad de Biofísica (CSIC, UPV/EHU), Departamento de Bioquímica, Universidad del País Vasco, 48940 Leioa, Spain Institut de Formation aux Carrieres de Sante de Rabat, 10000 Rabat, Morocco.
Hasna
H
Ahyayauch
Unidad de Biofísica (CSIC, UPV/EHU), Departamento de Bioquímica, Universidad del País Vasco, 48940 Leioa, Spain.
Alicia
A
Alonso
Department of Physics, Tampere University of Technology, FI-33101 Tampere, Finland MEMPHYS-Center for Biomembrane Physics, University of Southern Denmark, DK-5230 Odense M, Denmark.
Ilpo
I
Vattulainen
Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843.
Tatyana I
TI
Igumenova
Center for Plant Molecular Biology, Plant Physiology, Universität Tübingen, 72076 Tübingen, Germany vytas@tamhsc.edu gabriel.schaaf@zmbp.uni-tuebingen.de.
Gabriel
G
Schaaf
Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Sciences Center, Texas A&M University, College Station, TX 77843 Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843 Department of Chemistry, Texas A&M University, College Station, TX 77843 vytas@tamhsc.edu gabriel.schaaf@zmbp.uni-tuebingen.de.
Vytas A
VA
Bankaitis
D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000166:cytology / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000737:chemistry / Q000502:physiology*; D001665:Binding Sites; D002462:Cell Membrane / Q000502:physiology*; D016764:Cell Polarity; D056004:Molecular Dynamics Simulation; D009024:Morphogenesis; D019269:Phosphatidylinositol 4,5-Diphosphate / Q000378:metabolism*; D049294:Phospholipid Transfer Proteins / Q000737:chemistry / Q000502:physiology*; D018517:Plant Roots / Q000254:growth & development / Q000378:metabolism*; D011485:Protein Binding; D015398:Signal Transduction
D029681:Arabidopsis Proteins; D019269:Phosphatidylinositol 4,5-Diphosphate; D049294:Phospholipid Transfer Proteins; C000606246:Sfh1 protein, Arabidopsis