A <i>Plasmodium</i>‐like virulence effector of the soybean cyst nematode suppresses plant innate immunity

Noon, Jason B.; Qi, Mingsheng; Sill, Danielle N.; Muppirala, Usha; Akker, Sebastian Eves‐van den; Maier, Thomas R.; Dobbs, Drena; Mitchum, Melissa G.; Hewezi, Tarek; Baum, Thomas J.

doi:10.1111/nph.14047

Cited by 43 publications

(36 citation statements)

References 69 publications

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“…As the Hs4E02 effector gene is expressed in esophageal glands during all stages of infection (Patel et al ., ), we hypothesized that this effector has a role in the long‐term modulation of plant defenses. This hypothesis is supported by a recently published report showing that cyst nematode effector GLAND18, whose gene is also constitutively expressed in the esophageal glands throughout all life stages of the cyst nematode, strongly suppresses plant innate immune responses (Noon et al ., ).…”

Section: Resultsmentioning

confidence: 97%

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

et al. 2019

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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.

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Section: Resultsmentioning

confidence: 97%

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

et al. 2019

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“…A plant pathogen effector protein sharing a highly similar motif with Plasmodium spp. has been previously identified as the Plasmodium‐like virulence effector HgGLAND18, a suppressor of plant innate immunity from the soybean cyst nematode Heterodera glycines (Noon et al., ).…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis Identifies Plasmodiophora brassicae Secondary Infection Effector Candidates

Pérez‐López

Hossain

et al. 2020

J Eukaryotic Microbiology

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Plasmodiophora brassicae (Wor.) is an obligate intracellular plant pathogen affecting Brassicas worldwide. Identification of effector proteins is key to understanding the interaction between P. brassicae and its susceptible host plants. To date, there is very little information available on putative effector proteins secreted by P. brassicae during a secondary infection of susceptible host plants, resulting in root gall production. A bioinformatics pipeline approach to RNA-Seq data from Arabidopsis thaliana (L.) Heynh. root tissues at 17, 20, and 24 d postinoculation (dpi) identified 32 small secreted P. brassicae proteins (SSPbPs) that were highly expressed over this secondary infection time frame. Functional signal peptides were confirmed for 31 of the SSPbPs, supporting the accuracy of the pipeline designed to identify secreted proteins. Expression profiles at 0, 2, 5, 7, 14, 21, and 28 dpi verified the involvement of some of the SSPbPs in secondary infection. For seven of the SSPbPs, a functional domain was identified using Blast2GO and 3D structure analysis and domain functionality was confirmed for SSPbP22, a kinase localized to the cytoplasm and nucleus.

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“…The GLAND18 effector has sequence and functional similarity to an immunosuppressive effector of Plasmodium spp. (Noon et al, 2016). Cyst nematodes also target plant developmental pathways by secreting effector proteins that mimic CLAVATA3/ESR (CLE) signaling peptides of plants (Mitchum et al, 2012;Guo et al, 2017) that interact with receptor-like kinases to initiate developmental changes (Chen et al, 2015;Guo et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

et al. 2018

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Cyst nematodes deliver effector proteins into host cells to manipulate cellular processes and establish a metabolically hyperactive feeding site. The novel 30D08 effector protein is produced in the dorsal gland of parasitic juveniles, but its function has remained unknown. We demonstrate that expression of 30D08 contributes to nematode parasitism, the protein is packaged into secretory granules and it is targeted to the plant nucleus where it interacts with SMU2 (homolog of suppressor of mec-8 and unc-52 2), an auxiliary spliceosomal protein. We show that SMU2 is expressed in feeding sites and an smu2 mutant is less susceptible to nematode infection. In Arabidopsis expressing 30D08 under the SMU2 promoter, several genes were found to be alternatively spliced and the most abundant functional classes represented among differentially expressed genes were involved in RNA processing, transcription and binding, as well as in development, and hormone and secondary metabolism, representing key cellular processes known to be important for feeding site formation. In conclusion, we demonstrated that the 30D08 effector is secreted from the nematode and targeted to the plant nucleus where its interaction with a host auxiliary spliceosomal protein may alter the pre-mRNA splicing and expression of a subset of genes important for feeding site formation.

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A Plasmodium‐like virulence effector of the soybean cyst nematode suppresses plant innate immunity

Cited by 43 publications

References 69 publications

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

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

Transcriptome Analysis Identifies Plasmodiophora brassicae Secondary Infection Effector Candidates

The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

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