Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth

Abstract

Peptide-mediated cell-to-cell signaling has crucial roles in coordination and definition of cellular functions in plants. Peptide-receptor matching is important for understanding the mechanisms underlying peptide-mediated signaling. Here we report the structure-guided identification of root meristem growth factor (RGF) receptors important for plant development. An assay based on a signature ligand recognition motif (Arg-x-Arg) conserved in a subfamily of leucine-rich repeat receptor kinases (LRR-RKs) identified the functionally uncharacterized LRR-RK At4g26540 as a receptor of RGF1 (RGFR1). We further solved the crystal structure of RGF1 in complex with the LRR domain of RGFR1 at a resolution of 2.6 Å, which reveals that the Arg-x-Gly-Gly (RxGG) motif is responsible for specific recognition of the sulfate group of RGF1 by RGFR1. Based on the RxGG motif, we identified additional four RGFRs. Participation of the five RGFRs in RGF-induced signaling is supported by biochemical and genetic data. We also offer evidence showing that SERKs function as co-receptors for RGFs. Taken together, our study identifies RGF receptors and co-receptors that can link RGF signals with their downstream components and provides a proof of principle for structure-based matching of LRR-RKs with their peptide ligands.

RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana

“…Therefore, we believe that RGIs, at least RGI1, qualify as the receptors of RGF1. This conclusion is consistent with recent independent studies from two other research groups [55,56]. Matsubayashi's group used a photoaffinity approach and identified three RGF1 receptors in Arabidopsis [55], which are identical to our RGI1 to RGI3.…”

“…Finally, most of the characterized ligand-binding npg www.cell-research.com | Cell Research LRR-RLKs use BAK1 and its paralogs as their co-receptors. Consistently, biochemical analysis by Chai's group showed that these five LRR-RLKs can form heterodimers with SERK family members including BAK1 upon ligand induction and genetic studies further confirmed that these SERKs serve as co-receptors in this signaling pathway [56].…”

“…Matsubayashi's group used a photoaffinity approach and identified three RGF1 receptors in Arabidopsis [55], which are identical to our RGI1 to RGI3. On the other hand, Chai's group identified the same 5 RGF1 receptors as we show here based on the presence of conserved RXR and RXGG signature motifs in the extracellular domains of these receptors [56]. The RXR and RXGG motifs can interact with the C-terminal asparagine residue and the sulfate group of RGF1, respectively.…”

“…The RXR and RXGG motifs can interact with the C-terminal asparagine residue and the sulfate group of RGF1, respectively. In addition, they solved the structure of the RGF1-At4G26540 complex (equivalent to our RGI3) at a resolution of 2.6 Å [56].…”

Peptide signaling in plants: finding partners is the key

“…Different from the genetic strategy used by Ou et al [9], Song et al [10] identified the same LRR-RLKs as the RGF receptors (called RGFRs) by taking a "signature motif-guided" structure approach [10]. Their previous study npg and appears to determine the specificity of their interaction with RGF peptides.…”