Identification of Open Stomata1-Interacting Proteins Reveals Interactions with Sucrose Non-fermenting1-Related Protein Kinases2 and with Type 2A Protein Phosphatases That Function in Abscisic Acid Responses

Rainer Waadt; Bianca Manalansan; Navin Rauniyar; Shintaro Munemasa; Matthew A Booker; Benjamin Brandt; Christian Waadt; Dmitri A Nusinow; Steve A Kay; Hans-Henning Kunz; Karin Schumacher; Alison DeLong; John R Yates, 3rd; Julian I Schroeder

doi:10.1104/pp.15.00575

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Identification of Open Stomata1-Interacting Proteins Reveals Interactions with Sucrose Non-fermenting1-Related Protein Kinases2 and with Type 2A Protein Phosphatases That Function in Abscisic Acid Responses

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Identification of Open Stomata1-Interacting Proteins Reveals Interactions with Sucrose Non-fermenting1-Related Protein Kinases2 and with Type 2A Protein Phosphatases That Function in Abscisic Acid Responses

Rainer Waadt, Bianca Manalansan, Navin Rauniyar, Shintaro Munemasa, Matthew A Booker, Benjamin Brandt, Christian Waadt, Dmitri A Nusinow, Steve A Kay, Hans-Henning Kunz, …

Plant physiology (Bethesda), Vol.169(1), pp.760-779

09/2015

DOI: https://doi.org/10.1104/pp.15.00575

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https://hdl.handle.net/2376/110260

PMID: 26175513

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Abstract

Germination - drug effects

Protein Kinases - metabolism

Reproducibility of Results

Immunoprecipitation

Protein Interaction Maps - drug effects

Fluorescence

Mutation - genetics

Protein Subunits - metabolism

Arabidopsis Proteins - metabolism

Abscisic Acid - pharmacology

Two-Hybrid System Techniques

Plants, Genetically Modified

Protein Binding - drug effects

Protein Phosphatase 2 - metabolism

Protein Multimerization - drug effects

Protein-Serine-Threonine Kinases - metabolism

The plant hormone abscisic acid (ABA) controls growth and development and regulates plant water status through an established signaling pathway. In the presence of ABA, pyrabactin resistance/regulatory component of ABA receptor proteins inhibit type 2C protein phosphatases (PP2Cs). This, in turn, enables the activation of Sucrose Nonfermenting1-Related Protein Kinases2 (SnRK2). Open Stomata1 (OST1)/SnRK2.6/SRK2E is a major SnRK2-type protein kinase responsible for mediating ABA responses. Arabidopsis (Arabidopsis thaliana) expressing an epitope-tagged OST1 in the recessive ost1-3 mutant background was used for the copurification and identification of OST1-interacting proteins after osmotic stress and ABA treatments. These analyses, which were confirmed using bimolecular fluorescence complementation and coimmunoprecipitation, unexpectedly revealed homo- and heteromerization of OST1 with SnRK2.2, SnRK2.3, OST1, and SnRK2.8. Furthermore, several OST1-complexed proteins were identified as type 2A protein phosphatase (PP2A) subunits and as proteins involved in lipid and galactolipid metabolism. More detailed analyses suggested an interaction network between ABA-activated SnRK2-type protein kinases and several PP2A-type protein phosphatase regulatory subunits. pp2a double mutants exhibited a reduced sensitivity to ABA during seed germination and stomatal closure and an enhanced ABA sensitivity in root growth regulation. These analyses add PP2A-type protein phosphatases as another class of protein phosphatases to the interaction network of SnRK2-type protein kinases.

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Title: Identification of Open Stomata1-Interacting Proteins Reveals Interactions with Sucrose Non-fermenting1-Related Protein Kinases2 and with Type 2A Protein Phosphatases That Function in Abscisic Acid Responses
Creators: Rainer Waadt - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Bianca Manalansan - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Navin Rauniyar - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Shintaro Munemasa - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Matthew A Booker - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Benjamin Brandt - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Christian Waadt - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Dmitri A Nusinow - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Steve A Kay - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Hans-Henning Kunz - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Karin Schumacher - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Alison DeLong - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
John R Yates, 3rd - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.)
Julian I Schroeder - Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, California 92093-0116 (R.W., B.M., S.M., B.B., H.-H.K., J.I.S.);Centre for Organismal Studies, Plant Developmental Biology, University of Heidelberg, 69120 Heidelberg, Germany (R.W., K.S.);Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037 (N.R., J.R.Y.);Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.);Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, Rhode Island 02912 (M.A.B., A.D.);Department of Biology, Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.A.N.); andMolecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089 (S.A.K.) jischroeder@ucsd.edu
Publication Details: Plant physiology (Bethesda), Vol.169(1), pp.760-779
Academic Unit: Biological Sciences, School of
Publisher: United States
Grant note: T32 GM007601 / NIGMS NIH HHS P41 GM103533 / NIGMS NIH HHS R01 GM060396 / NIGMS NIH HHS R01GM056006 / NIGMS NIH HHS R01 GM067837 / NIGMS NIH HHS GM060396 / NIGMS NIH HHS F32 GM083585 / NIGMS NIH HHS F32GM083585 / NIGMS NIH HHS R01GM067837 / NIGMS NIH HHS R01 GM056006 / NIGMS NIH HHS
Identifiers: 99900546913801842
Language: English
Resource Type: Journal article