Re‐targeting of a plant defense protease by a cyst nematode effector

Abstract

Plants mount defense responses during pathogen attacks, and robust host defense suppression by pathogen effector proteins is essential for infection success. 4E02 is an effector of the sugar beet cyst nematode Heterodera schachtii. Arabidopsis thaliana lines expressing the effector-coding sequence showed altered expression levels of defense response genes, as well as higher susceptibility to both the biotroph H. schachtii and the necrotroph Botrytis cinerea, indicating a potential suppression of defenses by 4E02. Yeast two-hybrid analyses showed that 4E02 targets A. thaliana vacuolar papain-like cysteine protease (PLCP) 'Responsive to Dehydration 21A' (RD21A), which has been shown to function in the plant defense response. Activity-based protein profiling analyses documented that the in planta presence of 4E02 does not impede enzymatic activity of RD21A. Instead, 4E02 mediates a re-localization of this protease from the vacuole to the nucleus and cytoplasm, which is likely to prevent the protease from performing its defense function and at the same time, brings it in contact with novel substrates. Yeast two-hybrid analyses showed that RD21A interacts with multiple host proteins including enzymes involved in defense responses as well as carbohydrate metabolism. In support of a role in carbohydrate metabolism of RD21A after its effector-mediated relocalization, we observed cell wall compositional changes in 4E02 expressing A. thaliana lines. Collectively, our study shows that 4E02 removes RD21A from its defense-inducing pathway and repurposes this enzyme by targeting the active protease to different cell compartments.

Plant Proteins and Processes Targeted by Parasitic Nematode Effectors

“…A third striking example is provided by PLCPs, which constitute key hubs in plant immunity (Misas-Villamil et al, 2016). PLCPs are targeted by M. chitwoodi Mc01194 (Davies et al, 2015) and CN G. rostochiensis GrVAP-1 and H. schachtii Hs4E02 (Lozano-Torres et al, 2012; Pogorelko et al, 2019) effectors in diverse host plants. Mc01194 and Hs4E02 target the same Arabidopsis PLCP, “Responsive to Dehydration 21A” (RD21A), to promote parasitism (Davies et al, 2015; Pogorelko et al, 2019).…”

“…PLCPs are targeted by M. chitwoodi Mc01194 (Davies et al, 2015) and CN G. rostochiensis GrVAP-1 and H. schachtii Hs4E02 (Lozano-Torres et al, 2012; Pogorelko et al, 2019) effectors in diverse host plants. Mc01194 and Hs4E02 target the same Arabidopsis PLCP, “Responsive to Dehydration 21A” (RD21A), to promote parasitism (Davies et al, 2015; Pogorelko et al, 2019). The expression of G. rostochiensis VAP1, which targets RCR3 Pim in tomato, promotes susceptibility to G. rostochiensis and to the leaf mold Cladosporium fulvum (Lozano-Torres et al, 2012).…”

PbMC1a/1b regulates lignification during stone cell development in pear (Pyrus bretschneideri) fruit

“…RD21 shows a change in its subcellular localization when interacting with proteins. Hs4E02 is located in the nucleus, causing RD21A to accumulate in different cell compartments, and interaction is observed in the cytoplasm as well as the nucleus 55 . AtSerpin1 is a protease that inhibits AtMC1-mediated cell death and colocalizes in the cytoplasm and nucleus 56 .…”

Cleavage of a pathogen apoplastic protein by plant subtilases activates immunity

“…More recently, a study on the pathogenicity of Huanglongbing uncovered the Candidatus Liberibacter asiaticus effector SDE1 that directly interacts with and inhibits citrus PLCP activity(Clark et al, 2018). In another case, the cyst nematode Heterodera schachtii effector protein 4E02 repurposes a PLCP from its role in defense by targeting it to distinct plant cell compartments without inhibibiting its activity(Pogorelko et al, 2019). These studies illustrate a concerted interaction between the host proteases and the pathogen protease inhibitors, which dictates the success of pathogen colonization.…”