Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/27/2010
Publication Date: 2/1/2011
Citation: Wang, J., Replogle, A., Hussey, R., Baum, T., Wang, X., Davis, E.L., Mitchum, M.G. 2011. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Molecular Plant Pathology. 12:177-186. Interpretive Summary: The beet cyst nematode (BCN, Heterodera schachtii) can cause significant yield losses on a variety of crop plants, such as sugar beet, garden beet, spinach, broccoli, cauliflower, cabbage, radish, etc. This nematode pest attacks plant roots and feeds on modified root cells that provide the necessary nutrients to the developing nematode. This paper reports the identification of two CLAVATA3/ESR (CLE)-like genes (HsCLE1 and HsCLE2) from BCN. These nematode CLE genes encode secreted proteins sharing structural similarity to plant CLE peptides. Results from the in-depth functional characterization of these two nematode CLE genes revealed that these nematode produced CLE proteins have a similar function as plant CLE peptides, suggesting that the beet cyst nematode may use mimicry of plant CLE peptides to promote a successful infection on host plants. This study also indicated potential target plant peptides mimicked by these nematode CLEs. Knowledge obtained from this study may help identify host plant targets useful for generating novel nematode resistance in crop plants.
Technical Abstract: In this article, we present the cloning of two CLAVATA3/ESR (CLE)-like genes, HsCLE1 and HsCLE2, from the beet cyst nematode Heterodera schachtii, a plant-parasitic cyst nematode with a relatively broad host range that includes the model plant Arabidopsis. CLEs are small secreted peptide ligands that play important roles in plant growth and development. By secreting peptide mimics of plant CLEs, the nematode can developmentally reprogram root cells for the formation of unique feeding sites within host roots for its own benefit. Both HsCLE1 and HsCLE2 encode small secreted polypeptides with a conserved C-terminal CLE domain sharing highest similarity to Arabidopsis CLEs 1–7. Moreover, HsCLE2 contains a 12-amino-acid CLE motif that is identical to AtCLE5 and AtCLE6. Like all other plant and nematode CLEs identified to date, HsCLEs caused wuschel-like phenotypes when overexpressed in Arabidopsis, and this activity was abolished when the proteins were expressed without the CLE motif. HsCLEs could also function in planta without a signal peptide, highlighting the unique, yet conserved function of nematode CLE variable domains in trafficking CLE peptides for secretion. In a direct comparison of HsCLE2 overexpression phenotypes with those of AtCLE5 and AtCLE6, similar shoot and root phenotypes were observed. Exogenous application of 12-aminoacid synthetic peptides corresponding to the CLE motifs of HsCLEs and AtCLE5/6 suggests that the function of this class of CLEs may be subject to complex endogenous regulation. When seedlings were grown on high concentrations of peptide (10 mM), root growth was suppressed; however, when seedlings were grown on low concentrations of peptide (0.1 mM), root growth was stimulated. Together, these findings indicate that AtCLEs1–7 may be the target peptides mimicked by HsCLEs to promote parasitism.