Abstract
Plasmodiophora brassicae is a devastating obligate, intracellular, biotrophic pathogen that causes clubroot disease in crucifer plants. Disease progression is regulated by effector proteins secreted by P. brassicae. Twelve P. brassicae putative effectors (PbPEs), expressed at various stages of disease development [0, 2, 5, 7, 14, 21, and 28 days post inoculation (DPI)] in Arabidopsis and localizing to the plant endomembrane system, were studied for their roles in pathogenesis. Of the 12 PbPEs, seven showed an inhibitory effect on programmed cell death (PCD) as triggered by the PCD inducers, PiINF1 (Phytophthora infestans Infestin 1) and PiNPP1 (P. infestans necrosis causing protein). Showing the strongest level of PCD suppression, PbPE15, a member of the 2-oxoglutarate (2OG) and Fe (II)-dependent oxygenase superfamily and with gene expression during later stages of infection, appears to have a role in tumorigenesis as well as defense signaling in plants. PbPE13 produced an enhanced PiINF1-induced PCD response. Transient expression, in Nicotiana benthamiana leaves of these PbPEs minus the signal peptide (SP) (ΔspPbPEGFPs), showed localization to the endomembrane system, targeting the endoplasmic reticulum (ER), Golgi bodies and nucleo-cytoplasm, suggesting roles in manipulating plant cell secretion and vesicle trafficking. ΔspPbPE13GFP localized to plasma membrane (PM) lipid rafts with an association to plasmodesmata, suggesting a role at the cell-to-cell communication junction. Membrane relocalization of ΔspPbPE13GFP, triggered by flagellin N-terminus of Pseudomonas aeruginosa (flg22 – known to elicit a PAMP triggered immune response in plants), supports its involvement in raft-mediated immune signaling. This study is an important step in deciphering P. brassicae effector roles in the disruption of plant immunity to clubroot disease.
Highlights
Plasmodiophora brassicae is the intracellular obligate biotrophic plant pathogen responsible for clubroot disease in the Brassicaceae
From a cDNA library generated from canola galls, we have identified a number of P. brassicae effectors that, by localizing to different sub-compartments of the plant cell endomembrane system, as well as the manipulation of plant-triggered programmed cell death (PCD), suggest a role in a successful P. brassicae infection and colonization of the plant root
Selection of Plasmodiophora brassicae Candidate Effectors cDNAs from a full-length cDNA library of total RNAs extracted from P. brassicae-infected canola galls at 35 days post inoculation (DPI) with P. brassicae resting spores were sequenced and screened for P. brassicae putative effectors (PbPEs)
Summary
Plasmodiophora brassicae is the intracellular obligate biotrophic plant pathogen responsible for clubroot disease in the Brassicaceae. Secondary infection is crucial to the completion of the P. brassicae life cycle and the production of the next-generation of resting spores. To facilitate the colonization of a plant root, P. brassicae secretes effector proteins to manipulate or interfere with the pathogen-induced host processes (Schwelm et al, 2015). Putative P. brassicae effector proteins, expressed during primary infection in canola as well as a secondary infection in Arabidopsis, have been identified through transcriptome analysis (Pérez-López et al, 2018, 2020; Chen et al, 2019). More recent reports have identified a P. brassicae MAPKKK protein as an elicitor for the generation of ROS and hypersensitive response (HR)-like cell death after transient expression in Nicotiana benthamiana (Jin et al, 2020) and a P. brassicae cysteine protease inhibitor SSPbP53 that targets cruciferous papain-like cysteine proteases to manipulate plant immunity (Pérez-López et al, Unpublished results)
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