Retargeting of a plant defense protease by a cyst nematode effector

Authors: POGORELKO, GENNADY - Iowa State University; JUVALE, PARIJAT - Iowa State University; Rutter, William; HUTTEN, MARION - University Of Bonn; MAIER, THOMAS - Iowa State University; HEWEZI, TAREK - University Of Tennessee; PAULUS, JUDITH - University Of Oxford; VAN DER HOORN, RENIER - Oxford University; GRUNDLER, FLORIAN - University Of Bonn; SIDDIQUE, SHAHID - University Of Bonn; LIONETTI, VINCENZO - University Of Roma; ZABOTINA, OLGA - Iowa State University; BAUM, THOMAS - Iowa State University

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/15/2019
Publication Date: 2/23/2019
Citation: Pogorelko, G., Juvale, P., Rutter, W.B., Hutten, M., Maier, T., Hewezi, T., Paulus, J., Van Der Hoorn, R., Grundler, F., Siddique, S., Lionetti, V., Zabotina, O., Baum, T. 2019. Retargeting of a plant defense protease by a cyst nematode effector. Plant Journal. https://doi.org/10.1111/tpj.14295.
DOI: https://doi.org/10.1111/tpj.14295

Interpretive Summary: The sugar beet cyst nematode causes significant yield losses in sugar beet farming operations, and is a close relative of the soybean cyst nematode which is among the most economically important pathogens of soybean in the United States. One of the proteins (effectors) secreted by both of these cyst nematode species into their respective host plants is called 4E02. Although it has been known for some time that 4E02 is transported to the nucleus of a host plant cell during infection, it has never been fully understood how this nematode protein functions in a host plant cell to promote cyst nematode parasitism. In this manuscript, a USDA-ARS scientist from the U.S. Vegetable Laboratory in Charleston, South Carolina, in collaboration with scientists from Iowa State University, the University of Tennessee, the University of Oxford, and Bonn University in Germany present evidence that 4E02 has a novel virulence mechanism that has never before been documented in nematodes. This evidence shows that 4E02 targets and interacts with a plant protein that is normally involved in defense responses (RD21A), and relocates this protein to the plant cell nucleus where it is not normally found, and where we show that this plant protein now performs novel functions that ultimately helps the nematode to infect its host plant. The discovery of this novel virulence function furthers our understanding of how cyst nematodes are able to successfully infect and manipulate their host plants. This accomplishment contributes to our overall goal of developing crop plants with resistance to these nematode pests in the field.

Technical Abstract: Plants mount defense responses during pathogen attacks, and robust host defense suppression by the pathogens is essential for infection success. The 4E02 effector of the sugar beet cyst nematode Heterodera schachtii targets Arabidopsis vacuolar papain-like cysteine protease 'Responsive to Dehydration 21A' (RD21A), which functions in the plant defense response. While 4E02 interacts with the RD21A region containing its active site, in planta presence of this effector does not impede enzymatic activity of this protease. Instead, 4E02 mediates a re-localization of this vacuolar protease to the nucleus and cytoplasm, which likely prevents the protease from performing its defense function and at the same time brings it in contact with novel substrates. In order to identify RD21A substrates we show that this protease interacts with multiple host proteins including enzymes involved in defense responses as well as carbohydrate metabolism. In support of these pleiotropic effects of RD21A as a function of 4E02, we detected altered expression levels of defense response genes as well as higher susceptibility to H. schachtii in Arabidopsis lines expressing the effector coding sequence. Furthermore, we observed cell wall compositional changes in these lines. Not only does 4E02 remove RD21A from its defense-inducing pathway, by targeting the active protease to a new compartment, this enzyme is repurposed in a manner not previously documented.