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Synergistic Interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in Cyst Nematode Parasitism of Arabidopsis

¹Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia 65211, U.S.A.; ²RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; ³Department of Molecular and Cellular Biology and School of Plant Sciences, University of Arizona, Tucson 85721, U.S.A.; ⁴United States Department of Agriculture–Agricultural Research Service, Robert W. Holley Center for Agriculture and Health and Department of Plant Pathology and Plant–Microbe Biology, Cornell University, Ithaca, NY 14853, U.S.A.; ⁵Graduate School of Science and Technology, Kumamoto University, Kumamoto, Japan

Plant-parasitic cyst nematodes secrete CLAVATA3 (CLV3)/ENDOSPERM SURROUNDING REGION (CLE)-like effector proteins. These proteins act as ligand mimics of plant CLE peptides and are required for successful nematode infection. Previously, we showed that the CLV2/CORYNE (CRN) heterodimer receptor complex is required for nematode CLE signaling. However, there was only a partial reduction in nematode infection when this signaling was disrupted, indicating that there might be additional nematode CLE receptors. In this study, we demonstrate that CLV1 and RECEPTOR-LIKE PROTEIN KINASE 2/TOADSTOOL2 (RPK2), two additional receptors that can transmit the CLV3 signal independent of CLV2/CRN for shoot apical meristem maintenance, also play a role in nematode CLE perception. Localization studies showed that both receptors are expressed in nematode-induced syncytia. Infection assays with clv1 and rpk2 single mutants revealed a decrease in both nematode infection and syncytium size. Significantly, further reduction in nematode infection was observed when rpk2 was combined with clv1 and clv2 mutants. Taken together, our results indicate that parallel signaling pathways involving CLV1, CLV2, and RPK2 are important for nematode parasitism.