|CHEN, SHIYAN - Cornell University - New York|
|LANG, PING - Cornell University - New York|
|CHRONIS, DEMOTHENIS - Former ARS Employee|
|ZHANG, SHENG - Cornell University - New York|
|DEJONG, WALTER - Cornell University - New York|
|MITCHUM, MELISSA - University Of Missouri|
Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2014
Publication Date: 11/21/2014
Citation: Chen, S., Lang, P., Chronis, D., Zhang, S., Dejong, W., Mitchum, M., Wang, X. 2014. In planta processing and glycosylation of a nematode CLE effector and its interaction with a CLV2-like receptor to promote parasitism. Plant Physiology. 167:262-272.
Interpretive Summary: Plant-parasitic cyst nematodes are among the most devastating plant pathogens causing substantial crop losses globally. Cyst nematodes secrete effector proteins that mimic plant CLAVATA3/ESR (CLE)-like peptide hormones into the roots of host plants to facilitate successful infection. In this study, we show for the first time that a CLE effector secreted from the potato cyst nematode (Globodera rostochiensis) during infection is recognized by plant cellular machinery to become a bioactive CLE peptide that interacts with a receptor from potato (StCLV2) to promote nematode infection. This study not only reveals a specific molecular interaction that underpins the basis of CLE mimicry in nematode parasitism of host plants but also contributes to understanding the biology of CLE peptide function in plants. The knowledge developed from this study suggests that the plant CLE signaling pathways may be targeted for generating novel nematode resistance in crop plants.
Technical Abstract: Like other biotrophic plant pathogens, plant-parasitic nematodes secrete effector proteins into host cells to facilitate infection. Effector proteins that mimic plant CLAVATA3/ESR (CLE)-like proteins have been identified in several cyst nematodes including the potato cyst nematode (PCN); however, the mechanistic details of this cross-kingdom mimicry are poorly understood. Plant CLEs are proteolytically processed and post-translationally modified to function as bioactive ligands critical to various aspects of plant development. Using ectopic expression coupled with nanoLC-MS/MS analysis, we show that the in planta mature form of proGrCLE1, a multi-domain CLE effector secreted by PCN during infection, is a 12-amino-acid arabinosylated glycopeptide (named GrCLE1-1Hyp4,7g) with striking structural similarity to mature plant CLE peptides. This glycopeptide is more resistant to hydrolytic degradation and binds with higher affinity to a CLV2-like receptor (StCLV2) from potato than its non-glycosylated form. We further show that StCLV2 is highly up-regulated at nematode infection sites and that transgenic potatoes with reduced StCLV2 expression are less susceptible to PCN infection. These results provide direct evidence that nematode-secreted CLE effectors are recognized by host cellular machinery to become bioactive mimics of endogenous plant CLE signals and suggest that interfering with the CLV2-mediated signaling pathway may confer nematode resistance in crop plants. Our results further highlight the significance of glycosylation in CLE signaling as well as in regulating CLE effector activity. Our finding that a multi-domain CLE is processed and modified similarly to single-domain CLEs provide new insight into CLE maturation in plants.