Receptor kinase-mediated control of primary active proton pumping at the plasma membrane

Anja Thoe Fuglsang; Astrid Kristensen; Tracey A. Cuin; Waltraud X. Schulze; Rolf Jörgen Persson; Kristina Heinsbæk Thuesen; Cecilie Karkov Ytting; Christian Berg Oehlenschlæger; Khalid Mahmood; Teis Esben Søndergaard; Sergey Shabala; Michael Broberg Palmgren

doi:10.1111/tpj.12680

Receptor kinase-mediated control of primary active proton pumping at the plasma membrane

Anja Thoe Fuglsang^*, Astrid Kristensen, Tracey A. Cuin, Waltraud X. Schulze, Rolf Jörgen Persson, Kristina Heinsbæk Thuesen, Cecilie Karkov Ytting, Christian Berg Oehlenschlæger, Khalid Mahmood, Teis Esben Søndergaard, Sergey Shabala, Michael Broberg Palmgren

^*Corresponding author for this work

60 Citations (Scopus)

Abstract

Acidification of the cell wall space outside the plasma membrane is required for plant growth and is the result of proton extrusion by the plasma membrane-localized H⁺-ATPases. Here we show that the major plasma membrane proton pumps in Arabidopsis, AHA1 and AHA2, interact directly in vitro and in planta with PSY1R, a receptor kinase of the plasma membrane that serves as a receptor for the peptide growth hormone PSY1. The intracellular protein kinase domain of PSY1R phosphorylates AHA2/AHA1 at Thr-881, situated in the autoinhibitory region I of the C-terminal domain. When expressed in a yeast heterologous expression system, the introduction of a negative charge at this position caused pump activation. Application of PSY1 to plant seedlings induced rapid in planta phosphorylation at Thr-881, concomitant with an instantaneous increase in proton efflux from roots. The direct interaction between AHA2 and PSY1R observed might provide a general paradigm for regulation of plasma membrane proton transport by receptor kinases.

Original language	English
Journal	Plant Journal
Volume	80
Issue number	6
Pages (from-to)	951-964
Number of pages	14
ISSN	0960-7412
DOIs	https://doi.org/10.1111/tpj.12680
Publication status	Published - 2014

Keywords

apoplastic pH
cell elongation
H pump
LRR kinase
peptide signalling

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@article{42729c824efb4dfba90e05270f84ab77,

title = "Receptor kinase-mediated control of primary active proton pumping at the plasma membrane",

abstract = "Acidification of the cell wall space outside the plasma membrane is required for plant growth and is the result of proton extrusion by the plasma membrane-localized H+-ATPases. Here we show that the major plasma membrane proton pumps in Arabidopsis, AHA1 and AHA2, interact directly in vitro and in planta with PSY1R, a receptor kinase of the plasma membrane that serves as a receptor for the peptide growth hormone PSY1. The intracellular protein kinase domain of PSY1R phosphorylates AHA2/AHA1 at Thr-881, situated in the autoinhibitory region I of the C-terminal domain. When expressed in a yeast heterologous expression system, the introduction of a negative charge at this position caused pump activation. Application of PSY1 to plant seedlings induced rapid in planta phosphorylation at Thr-881, concomitant with an instantaneous increase in proton efflux from roots. The direct interaction between AHA2 and PSY1R observed might provide a general paradigm for regulation of plasma membrane proton transport by receptor kinases.",

keywords = "apoplastic pH, cell elongation, H pump, LRR kinase, peptide signalling",

author = "Fuglsang, {Anja Thoe} and Astrid Kristensen and Cuin, {Tracey A.} and Schulze, {Waltraud X.} and Persson, {Rolf J{\"o}rgen} and Thuesen, {Kristina Heinsb{\ae}k} and Ytting, {Cecilie Karkov} and Oehlenschl{\ae}ger, {Christian Berg} and Khalid Mahmood and S{\o}ndergaard, {Teis Esben} and Sergey Shabala and Palmgren, {Michael Broberg}",

year = "2014",

doi = "10.1111/tpj.12680",

language = "English",

volume = "80",

pages = "951--964",

journal = "Plant Journal",

issn = "0960-7412",

publisher = "Wiley-Blackwell",

number = "6",

}

TY - JOUR

T1 - Receptor kinase-mediated control of primary active proton pumping at the plasma membrane

AU - Fuglsang, Anja Thoe

AU - Kristensen, Astrid

AU - Cuin, Tracey A.

AU - Schulze, Waltraud X.

AU - Persson, Rolf Jörgen

AU - Thuesen, Kristina Heinsbæk

AU - Ytting, Cecilie Karkov

AU - Oehlenschlæger, Christian Berg

AU - Mahmood, Khalid

AU - Søndergaard, Teis Esben

AU - Shabala, Sergey

AU - Palmgren, Michael Broberg

PY - 2014

Y1 - 2014

N2 - Acidification of the cell wall space outside the plasma membrane is required for plant growth and is the result of proton extrusion by the plasma membrane-localized H+-ATPases. Here we show that the major plasma membrane proton pumps in Arabidopsis, AHA1 and AHA2, interact directly in vitro and in planta with PSY1R, a receptor kinase of the plasma membrane that serves as a receptor for the peptide growth hormone PSY1. The intracellular protein kinase domain of PSY1R phosphorylates AHA2/AHA1 at Thr-881, situated in the autoinhibitory region I of the C-terminal domain. When expressed in a yeast heterologous expression system, the introduction of a negative charge at this position caused pump activation. Application of PSY1 to plant seedlings induced rapid in planta phosphorylation at Thr-881, concomitant with an instantaneous increase in proton efflux from roots. The direct interaction between AHA2 and PSY1R observed might provide a general paradigm for regulation of plasma membrane proton transport by receptor kinases.

AB - Acidification of the cell wall space outside the plasma membrane is required for plant growth and is the result of proton extrusion by the plasma membrane-localized H+-ATPases. Here we show that the major plasma membrane proton pumps in Arabidopsis, AHA1 and AHA2, interact directly in vitro and in planta with PSY1R, a receptor kinase of the plasma membrane that serves as a receptor for the peptide growth hormone PSY1. The intracellular protein kinase domain of PSY1R phosphorylates AHA2/AHA1 at Thr-881, situated in the autoinhibitory region I of the C-terminal domain. When expressed in a yeast heterologous expression system, the introduction of a negative charge at this position caused pump activation. Application of PSY1 to plant seedlings induced rapid in planta phosphorylation at Thr-881, concomitant with an instantaneous increase in proton efflux from roots. The direct interaction between AHA2 and PSY1R observed might provide a general paradigm for regulation of plasma membrane proton transport by receptor kinases.

KW - apoplastic pH

KW - cell elongation

KW - H pump

KW - LRR kinase

KW - peptide signalling

U2 - 10.1111/tpj.12680

DO - 10.1111/tpj.12680

M3 - Journal article

C2 - 25267325

AN - SCOPUS:84916638439

SN - 0960-7412

VL - 80

SP - 951

EP - 964

JO - Plant Journal

JF - Plant Journal

IS - 6

ER -

Receptor kinase-mediated control of primary active proton pumping at the plasma membrane

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Keywords

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