Activation of the LRR Receptor-Like Kinase PSY1R Requires Transphosphorylation of Residues in the Activation Loop

Abstract

PSY1R is a leucine-rich repeat (LRR) receptor-like kinase (RLK) previously shown to act as receptor for the plant peptide hormone PSY1 (peptide containing sulfated tyrosine 1) and to regulate cell expansion. PSY1R phosphorylates and thereby regulates the activity of plasma membrane-localized H+-ATPases. While this mechanism has been studied in detail, little is known about how PSY1R itself is activated. Here we studied the activation mechanism of PSY1R. We show that full-length PSY1R interacts with members of the SERK co-receptor family in planta. We identified seven in vitro autophosphorylation sites on serine and threonine residues within the kinase domain of PSY1R using mass spectrometry. We furthermore show that PSY1R autophosphorylation occurs in trans and that the initial transphosphorylation takes place within the activation loop at residues Ser951, Thr959, and Thr963. While Thr959 and Thr963 are conserved among other related plant LRR RLKs, Ser951 is unique to PSY1R. Based on homology modeling we propose that phosphorylation of Ser951 stabilize the inactive conformation of PSY1R.

Plant plasma membrane‐resident receptors: Surveillance for infections and coordination for growth and development

“…Another example is the PSKR1 receptor that mobilizes SERK1, SERK2, and BAK1 to form a stable complex and regulate root growth and cell expansion in response to PSK (Wang et al, 2015). Furthermore, the PSY1R receptor is also able to interact with SERKs to mediate PSY1 signal transduction after phosphorylation, and subsequently regulate cell expansion and cell division (Oehlenschlaeger et al, 2017). In Arabidopsis, SERK1 and SERK2 are also known to play a role in embryogenesis (Albrecht et al, 2005).…”

“…Namely, the CLE peptide TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY (TDIF) is recognized by the TDIF RECEPTOR (TDR), also known as PHLOEM INTERCALATED WITH XYLEM (PXY) (Fisher and Turner, 2007; Hirakawa et al, 2008). Further, the receptors ROOT GROWTH FACTOR (RGF) RECEPTOR 1–5 (RGFR1 to RGFR5) recognize the peptide RGF leading to a fine‐tuned control of the root meristem development (Ou et al, 2016; Shinohara et al, 2016).…”

Receptor-like protein kinase-mediated signaling in controlling root meristem homeostasis

“…The pskr1 pskr2 psy1r triple mutants had reduced RAM size and root length (Amano et al 2007). A recent study showed that PSY1R and SERKs interacted with and transphosphorylated each other, suggesting that SERKs may act as the coreceptor of PSY1R, but more genetic and structural evidence is needed (Oehlenschlaeger et al 2017) (Fig. 3B).…”

Sulfated plant peptide hormones

“…Several peptide receptors heterodimerize with co-receptors of the SOMATIC EMBRYOGENESIS RECEPTOR KINASE family, as shown for the sulfated peptide receptors PSKR1, PSY1R, and RGFRs (Table 1), resulting in subsequent mutual transphosphorylation of the cytoplasmic kinase domains within the activation loops. Kinase activity of the receptor is essential for peptide signaling (Hartmann et al, 2014, 2015; Ladwig et al , 2015; Wang et al , 2015; Ma et al , 2016; Song et al, 2016, 2017; Hohmann et al , 2017; Kaufmann et al , 2017; Oehlenschlæger et al , 2017). In the case of CIF signaling, it has not yet been reported that SGN3 forms a dimer with a co-receptor; however, based on the extremely high ligand affinity to SGN3 as measured by isothermal titration calorimetry in the absence of a possible co-receptor, Doblas et al (2017) speculated that the paradigm of peptide receptor–co-receptor formation might not apply for SGN3 activation.…”