Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H⁺-ATPase, and BAK1

Abstract

Phytosulfokine (PSK) is perceived by the leucine-rich repeat receptor kinase PSKR1 and promotes growth in Arabidopsis thaliana. PSKR1 is coexpressed with the CYCLIC NUCLEOTIDE-GATED CHANNEL gene CNGC17. PSK promotes protoplast expansion in the wild type but not in cngc17. Protoplast expansion is likewise promoted by cGMP in a CNGC17-dependent manner. Furthermore, PSKR1-deficient protoplasts do not expand in response to PSK but are still responsive to cGMP, suggesting that cGMP acts downstream of PSKR1. Mutating the guanylate cyclase center of PSKR1 impairs seedling growth, supporting a role for PSKR1 signaling via cGMP in planta. While PSKR1 does not interact directly with CNGC17, it interacts with the plasma membrane-localized H + -ATPases AHA1 and AHA2 and with the BRI-associated receptor kinase 1 (BAK1). CNGC17 likewise interacts with AHA1, AHA2, and BAK1, suggesting that PSKR1, BAK1, CNGC17, and AHA assemble in a functional complex. Roots of deetiolated bak1-3 and bak1-4 seedlings were unresponsive to PSK, and bak1-3 and bak1-4 protoplasts expanded less in response to PSK but were fully responsive to cGMP, indicating that BAK1 acts in the PSK signal pathway upstream of cGMP. We hypothesize that CNGC17 and AHAs form a functional cation-translocating unit that is activated by PSKR1/BAK1 and possibly other BAK1/RLK complexes.

A Plant Phytosulfokine Peptide Initiates Auxin-Dependent Immunity through Cytosolic Ca2+ Signaling in Tomato

“…This suggests that the observed increases in cytosolic [Ca 2+ ] may be generated through the PSKR1 GC activity-induced opening of the cyclic nucleotidegated channel (Ladwig et al, 2015). It should be noted that tomato CaMs not only act as Ca 2+ sensors that bind YUCs, but they can also bind directly to the PSKR1 receptor at the kinase subdomain (Hartmann et al, 2014;Fischer et al, 2017).…”

“…cGMP is a potential activating ligand for cyclic nucleotide-gated channels in plants. These cation channels are thought to facilitate Ca 2+ and other cation fluxes (Ladwig et al, 2015). Intriguingly, Pep-AtPepR1 signaling leads to the expression of pathogen defense genes, and this is suggested to be mediated by the cGMP-activated Ca 2+ -conducting channel CNGC2 as well as the elevation of cytosolic Ca 2+ levels (Qi et al, 2010;Ma et al, 2012).…”

“…Similarly, brassinosteroid perception by the receptor At-BRI1 leads to immediate cGMP-dependent cytosolic Ca 2+ release in vivo, a process that was abolished when the CNGC2 gene was mutated in Arabidopsis (Zhao et al, 2013a). Interestingly, PSK not only promotes cell expansion via a cGMP-dependent pathway but also activates a cation channel protein encoded by CNGC17 in Arabidopsis (Ladwig et al, 2015). It is thus reasonable to hypothesize that the PSK receptors may induce an intracellular Ca 2+ burst at the cell surface, leading to an immune response in cells where this pathway is triggered.…”

A Developmental and Molecular View of Formation of Auxin-Induced Nodule-Like Structures in Land Plants

“…We identified several phytosulfokine receptors (LOC_Os02g05970.1, LOC_Os06g47760.1, LOC_Os04g57630.1, and LOC_Os07g01710.1) to be differentially expressed during NLS formation. PSK receptor proteins share great structural similarity to BRI1 and in fact require BR to regulate growth (Ladwig et al, 2015). It will be interesting to determine if these genes are functionally involved in NLS formation.…”

Ligand-Induced Receptor-like Kinase Complex Regulates Floral Organ Abscission in Arabidopsis

“…BAK1 and SERK4 also heterodimerize with Arabidopsis FLAGELLIN-SENSING 2 (FLS2), the bacterial flagellin receptor, and other immune sensors upon the cognate ligand perception (Chinchilla et al, 2007; Heese et al, 2007; Roux et al, 2011). In addition, BAK1, together with SERK1, SERK2 and SERK4, is involved in male gametophyte development, root growth, stomatal patterning and cell death control (Aan den Toorn et al, 2015; Ladwig et al, 2015; Liebrand et al, 2014; Meng et al, 2015; Wang et al, 2015). …”