Characterization and response of two potato receptor-like kinases to cyst nematode infection

Authors: CHEN, SHIYAN - Cornell University; MITCHUM, MELISSA - University Of Georgia; Wang, Xiaohong

Submitted to: Plant Signaling and Behavior
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/12/2022
Publication Date: 11/23/2022
Citation: Chen, S., Mitchum, M., Wang, X. 2022. Characterization and response of two potato receptor-like kinases to cyst nematode infection. Plant Signaling and Behavior. 17:1. https://doi.org/10.1080/15592324.2022.2148372.
DOI: https://doi.org/10.1080/15592324.2022.2148372

Interpretive Summary: Potato cyst nematodes (PCN; golden nematode and pale cyst nematode) are internationally recognized quarantine pests that pose a serious threat to the U.S. potato industry. These devastating pests secrete effector proteins including CLE (CLAVATA3/EMBRYO SURROUNDING REGION-RELATED) into the root tissue to induce disease. A better understanding of nematode effector function and their targeted proteins in the host plant is necessary for developing novel tools for nematode control. Our previous study showed that the potato StCLV2 (CLAVATA2 from Solanum tuberosum) receptor is involved in perceiving PCN-secreted CLE peptides and is required for PCN parasitism. In this study, we identified two additional potato receptors, StRPK2 (RECEPTOR-LIKE PROTEIN KINASE 2 from Solanum tuberosum) and StCLV1, and investigated their role in nematode parasitism using functional analyses. Our results showed that StRPK2, but not StCLV1, is responsive to nematode infection and that transgenic potato lines with reduced StRPK2 expression had increased resistance to PCN infection. Our study revealed an important role of StRPK2 in PCN parasitism and suggests that interference with nematode CLE signaling may be a viable means to engineer nematode resistance in crop plants including potato.

Technical Abstract: Plant-parasitic cyst nematodes (Heterodera and Globdoera spp.) secrete CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) effector proteins, which act as ligand mimics of plant CLE peptides to promote successful nematode infection. Previous studies of the Arabidopsis-beet cyst nematode (BCN; H. schachtii) pathosystem showed that Arabidopsis CLE receptors including CLAVATA1 (CLV1), CLV2, and RECEPTOR-LIKE PROTEIN KINASE 2 (RPK2) are required for BCN CLE signaling. Studies further revealed that nematode CLE signaling through GmCLV2 and StCLV2, an Arabidopsis CLV2 orthologue from soybean (Glycines max) and potato (Solanum tuberosum), respectively, is required for the soybean cyst nematode (SCN; H. glycines) and the potato cyst nematode (PCN; G. rostochiensis) to induce disease in their respective host plant. In this study, we identified and characterized two additional potato receptors, StRPK2 and StCLV1, homologues of Arabidopsis RPK2 and CLV1, from potato, host for a role in PCN parasitism. Using promoter-reporter lines we showed that both StRPK2 and StCLV1 are expressed in the potato root but vary in their spatial expression patterns. Interestingly, StRPK2 but not StCLV1 was found to be expressed and upregulated at PCN infection sites. Nematode infection assays on StRPK2-knockdown lines revealed a decrease in nematode infection. Collectively, our results suggest that parallel CLE signaling pathways involving StCLV2 and StRPK2 are important for PCN parasitism and that manipulation of nematode CLE signaling may represent a viable means to engineer nematode resistance in crop plants including potato.