|WANG, JIANYING - University Of Missouri|
|DHROSO, ANDI - Worcester Polytechnical Institute|
|LIU, XUNLIANG - University Of Georgia|
|BAUM, THOMAS - Iowa State University|
|HUSSEY, RICHARD - University Of Georgia|
|DAVIS, ERIC - North Carolina State University|
|KORKIN, DMITRY - Worcester State College|
|MITCHUM, MELISSA - University Of Missouri|
Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/2/2020
Publication Date: 6/22/2020
Citation: Wang, J., Dhroso, A., Liu, X., Baum, T., Hussey, R.S., Davis, E., Wang, X., Korkin, D., Mitchum, M. 2020. Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal. New Phytologist. https://doi.org/10.1111/nph.16765.
Interpretive Summary: Like other plant pathogens, plant-parasitic nematodes including soybean cyst and potato cyst nematodes secrete effector proteins into host plant cells to promote successful infection. Our previous studies have revealed a critical role of CLAVATA3/ESR (CLE) effectors in nematode parasitism. In this study, we have used serial deletion experiments to further dissect the function of cyst nematode-secreted CLE effectors. Results of the study showed that a 37 amino acid sequence (VDIT) within the variable domain of CLE effectors is involved in trafficking of CLE effectors from the cytoplasm to the extracellular space of host root cells. The trafficking function of VDIT was found to be conserved across plant species, functional across cell types, and capable of translocating other unrelated small peptides. This study has uncovered an important mechanism of CLE effector trafficking in plants and suggested points vulnerable for disruption to engineer nematode resistance in crop plants.
Technical Abstract: • Cyst nematodes induce a multicellular feeding site within roots called a syncytium. It remains unknown how root cells are primed for incorporation into the developing syncytium. Furthermore, it is an enigma how CLAVATA3/ESR (CLE) peptide effectors secreted into the cytoplasm of the initial feeding cell could have an effect on plant cells so distant from where the nematode is feeding as the syncytium expands. • Here we describe a novel translocation signal within nematode CLE effectors that is recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells. • We show that the translocation signal is functionally conserved across CLE effectors identified in nematode species spanning three genera and multiple plant species, operative across plant cell types, and can traffic other unrelated small peptides from the cytoplasm to the apoplast of host cells via a previously unknown post-translational mechanism of ER translocation. • Our results uncover an unprecedented mechanism of effector trafficking by any plant pathogen to date and illustrates how phytonematodes can deliver effector proteins into host cells and then hijack plant cellular processes for their export back out of the cell to function as external signaling molecules to distant cells.