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

Abstract

SUMMARYAcidification 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.

Auxin and Cellular Elongation

“…Several receptor-like kinases are also able to activate or repress AHA2 in a ligand-dependent manner by modifying the C-terminal phosphorylation status of AHAs (Fuglsang et al, 2014;Haruta et al, 2014). In the case of the plant PEPTIDE-CONTAINING SULFATED TYROSINE RECEPTOR1 (PSYR1), the binding to the peptide PSY1 (Amano et al, 2007) enhances AHA2 activity via its phosphorylation of Thr-881, consequently triggering cell elongation (Fuglsang et al, 2014).…”

“…In the case of the plant PEPTIDE-CONTAINING SULFATED TYROSINE RECEPTOR1 (PSYR1), the binding to the peptide PSY1 (Amano et al, 2007) enhances AHA2 activity via its phosphorylation of Thr-881, consequently triggering cell elongation (Fuglsang et al, 2014). On the other hand, in the case of the receptor-like kinase FER, the binding of RALF1 inhibits root growth via the phosphorylation of Ser-899 in AHA2 by an unknown kinase (Haruta et al, 2014).…”

Environmental and Genetic Factors Regulating Localization of the Plant Plasma Membrane H+-ATPase

“…Thr-947 of AHA2 and Thr-948 of AHA1 and 3) is key for regulating the ATPase by blue light and auxin (Fuglsang et al, 1999;Kinoshita and Shimazaki, 1999;Robertson et al, 2004;Takahashi et al, 2012;Spartz et al, 2014). Additional phosphorylation sites, such as Thr-881 and Ser-899 of AHA2, are also likely involved in the activity modulation and these may be independently regulated by various protein kinases and phosphatases that function in the signaling pathways initiated by receptor kinases such as FERONIA (FER) and PSY1R, in response to the cognate peptide ligands (Fuglsang et al, 2014;Haruta et al, 2014). The complexity of H + -ATPase regulation is further underscored by the recent observation that dephosphorylation at Thr-947 of AHA2 by a protein phosphatase, PP2C plays an important and unique role in growth regulation by proteins encoded by auxin-induced small auxin upregulated genes, suggesting that efforts in characterizing kinase-mediated phosphorylation may only be providing a partial understanding of the regulation of this enzyme (Spartz et al, 2014).…”

Metal Fluoride Inhibition of a P-type H+ Pump

“…For all PM H ϩ -ATPases examined to date, terminal autoinhibitory regions appear to keep the PM H ϩ -ATPases in the low activity basal state (10 -14), whereas the activated state is induced by post-translational modification of the autoinhibitory domains in a manner that is strictly dependent on the overall physiological status of the plant or fungal cell. The fungal PM H ϩ -ATPase is transformed from the basal to the activated state when glucose is supplied as a carbon source (15), whereas a multitude of environmental factors, such as blue light (16), microbial toxins (17), nutritional status (18), salt (19), signaling lipids (20), auxin (21), and peptide hormones (22), have been demonstrated to influence autoinhibition of the plant PM H ϩ -ATPase. In both systems, signal transduction cascades transform the pump from the basal state to its fully activated form, a process that typically involves cellular perception of the signal(s), phosphorylation of the PM H ϩ -ATPases at the terminal autoinhibitory regions, and structural rearrangements of the pump.…”