Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE

Abstract

SUMMARYPlant-parasitic cyst nematodes secrete CLAVATA3 (CLV3)/ESR (CLE)-like effector proteins. These proteins have been shown to act as ligand mimics of plant CLE peptides and are required for successful nematode infection; however, the receptors for nematode CLE-like peptides have not been identified. Here we demonstrate that CLV2 and CORYNE (CRN), members of the receptor kinase family, are required for nematode CLE signaling. Exogenous peptide assays and overexpression of nematode CLEs in Arabidopsis demonstrated that CLV2 and CRN are required for perception of nematode CLEs. In addition, promoter-reporter assays showed that both receptors are expressed in nematode-induced syncytia. Lastly, infection assays with receptor mutants revealed a decrease in both nematode infection and syncytium size. Taken together, our results indicate that perception of nematode CLEs by CLV2 and CRN is not only required for successful nematode infection but is also involved in the formation and/or maintenance of nematode-induced syncytia.

Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition

“…It has long been known that cyst nematodes secrete peptides that are structural and functional mimics of plant CLAVATA3/ENDOSPERM SURROUNDING REGION-related (CLE) peptides (Wang et al, 2001(Wang et al, , 2005Gao et al, 2003;Lu et al, 2009), with the latter being peptide hormones required for meristem maintenance and vascular differentiation (Fiers et al, 2007). The nematode CLE effectors are required for virulence (Patel et al, 2008), apparently by stimulating both the CLV2 and the CLV1 pathways (Replogle et al, 2011(Replogle et al, , 2013. Similarly, phytopathogenic root-knot nematodes encode peptides similar to plant C-TERMINAL ENCODED PEPTIDEs (CEPs) that are involved in the regulation of cell expansion (Bobay et al, 2013;Tavormina et al, 2015), although their roles in pathogenesis remain unknown.…”

Phytoplasma Effector SAP54 Induces Indeterminate Leaf-Like Flower Development in Arabidopsis Plants

“…Plant parasitic nematodes secrete effectors into the host root, including CLAVATA3 (CLV3)/embryo surrounding region-like effector proteins that function as ligand mimics. These effectors interact with the CLV2/CORYNE receptor complex, an interaction that is important to the successful formation of nematode-induced syncytia, which act as feeding sites from which the parasites obtain nutrition (Replogle et al, 2011). However, effectors that modulate flower development have not yet been identified.…”

The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions

“…Since the discovery of CLV3 (Clark et al, 1995;Ito et al, 2006;Kondo et al, 2006;Ohyama et al, 2009), (putative) CLE genes have been identified in dicots, monocots, mosses, and algae (Jun et al, 2008;Oelkers et al, 2008;Miwa et al, 2009;Zhang et al, 2014;Strabala et al, 2014), and they were shown to act on diverse developmental processes, including shoot and root meristem development, nodulation, embryo and endosperm development, regulation of root architecture in response to nutrients, and vascular development (Hobe et al, 2003;Fiers et al, 2005;Hirakawa et al, 2008;Stahl et al, 2009;Jun et al, 2010;Mortier et al, 2010;Lim et al, 2011;Reid et al, 2011;Fiume and Fletcher, 2012;Okamoto et al, 2013;Araya et al, 2014;Richards et al, 2015;T.-T. Xu et al, 2015). Strikingly, plant-parasitic cyst nematodes also secrete CLE-like effector proteins that are required for successful nematode infection (Wang et al, 2010Replogle et al, 2011;Miyawaki et al, 2013). 3D structure modeling demonstrated that CLV3, CLE1, CLE2, and CLE6 shared a similar arch-shaped molecular structure with conserved residues at the C terminus and middle region, suggesting that these regions could be involved in receptor selection and binding .…”