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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Emerging Pests and Pathogens Research » Research » Publications at this Location » Publication #330180

Title: Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation

item GUO, XIAOLI - University Of Missouri
item WANG, JIANYING - University Of Missouri
item GARDNER, MICHAEL - University Of Missouri
item FUKUDA, HIROO - University Of Tokyo
item KONDO, YUKI - University Of Tokyo
item ETCHELLS, PETER - University Of Durham
item Wang, Xiaohong
item MITCHUM, MELISSA - University Of Missouri

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2016
Publication Date: 2/3/2017
Citation: Guo, X., Wang, J., Gardner, M., Fukuda, H., Kondo, Y., Etchells, P., Wang, X., Mitchum, M.G. 2017. Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation. PLoS Pathogens. 13(2):e1006142.

Interpretive Summary: The agriculturally-important cyst nematodes secrete effector proteins including CLE effectors into root cells to promote successfully infection. Our previous studies showed that nematode-secreted CLE effectors act as plant A-type CLE peptides and are important for nematode parasitism. Research further showed that receptors CLV1, CLV2/CRN and RPK2 from Arabidopsis and soybean are involved in perceiving nematode CLE peptides to promote nematode feeding cell formation. However, the downstream signaling pathways that are required for feeding cell formation are unclear. In this study, we have identified a new group of CLE genes that are found to act as plant B-type CLEs from cyst nematodes. We further used Arabidopsis promoter-reporter lines and mutant lines to demonstrate that modulation of the vascular stem cell pathway via nematode CLE peptides contributes to nematode feeding cell formation. This study has increased our understanding of molecular plant-nematode interactions and extended our knowledge of plant peptide signaling in plant developmental biology.

Technical Abstract: Stem cells are important in the continuous formation of various tissues during postembryonic organogenesis. Stem cell pools in the SAM (shoot apical meristem), RAM (root apical meristem) and vascular procambium/cambium are regulated by CLE-receptor kinase-WOX signaling modules. Previous data showed that cyst nematode CLE-like effector proteins delivered into host cells through a stylet, act as ligand mimics of plant A-type CLE peptides and are pivotal for successful parasitism. Consistent with this finding, we demonstrated that CLE receptors CLAVATA1 (CLV1), the CLAVATA2 (CLV2)/CORYNE (CRN) heterodimer receptor complex and RECEPTOR-LIKE PROTEIN KINASE 2 (RPK2) from Arabidopsis and soybean, which transmit the CLV3 signal in the SAM, are required for perception of cyst nematode CLEs and proper feeding site formation. Here we report the identification of a new class of CLE peptides from cyst nematodes with functional similarity to the B-type CLE peptide TDIF (tracheary element differentiation inhibitory factor) encoded by the CLE41 and CLE44 genes in Arabidopsis. We further demonstrate that the TDIF-TDR (TDIF receptor)-WOX4 pathway, which promotes procambial meristem cell proliferation, is involved in beet cyst nematode Heterodera schachtii parasitism. We observed activation of the TDIF pathway in developing feeding sites, reduced nematode infection in cle41 and tdrwox4 mutants, and compromised syncytium size in cle41, tdr, wox4 and tdrwox4 mutants. By qRT-PCR and promoter:GUS analyses, we showed that the expression of WOX4 is decreased in a clv1-101clv2-101rpk2-5 mutant, suggesting WOX4 is a potential downstream target of nematode CLEs. Exogenous treatment with both nematode A-type and B-type CLE peptides induced massive cell proliferation in wild type roots, suggesting that the two types of CLEs may synergistically regulate cell proliferation during feeding site formation. These findings highlight an important role of the procambial cell proliferation pathway in cyst nematode feeding site formation.