Papain‐like cysteine proteases as hubs in plant immunity

Misas-Villamil, Johana C.; Hoorn, Renier A. L. van der; Doehlemann, Gunther

doi:10.1111/nph.14117

Cited by 148 publications

(150 citation statements)

References 49 publications

(77 reference statements)

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“…() who showed that A. thaliana mutants lacking the PLCPs PAP1, PAP4, and PAP, and in particular RD21A, were more susceptible to H. schachtii infection. Additionally, the critical roles in plant immunity played by the orthologous members of RD21A in various plant species such as C14 from tomato and N. benthamiana , and CP1 from corn have also been documented (Misas‐Villamil et al ., ). Therefore, we decided to examine this protein−protein interaction in detail.…”

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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“…The recognition of the L. maculans effectors AvrLm1 (Gout et al, 2006) and AvrLm2 (Ghanbarnia et al, 2015) by the R genes LepR3 (Larkan et al, 2013) and Rlm2 (Larkan et al, 2015), respectively, is known to involve at least two additional partner proteins in the membrane-bound signaling complex; SOBIR1 and BAK1 (Larkan et al, 2015; Ma and Borhan, 2015). Other host proteins may also be involved in the signaling complex, based on other plant interactions with apoplastic fungal pathogens (van der Hoorn and Kamoun, 2008; Stotz et al, 2014; Misas-Villamil et al, 2016). Subtle variation in either the expression or sequence of these partner proteins may account for the range of resistance responses observed.…”

Section: Discussionmentioning

confidence: 99%

Single R Gene Introgression Lines for Accurate Dissection of the Brassica - Leptosphaeria Pathosystem

Larkan

Lydiate

et al. 2016

Front. Plant Sci.

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Seven blackleg resistance (R) genes (Rlm1, Rlm2, Rlm3, Rlm4, LepR1, LepR2 & LepR3) were each introgressed into a common susceptible B. napus doubled-haploid (DH) line through reciprocal back-crossing, producing single-R gene introgression lines (ILs) for use in the pathological and molecular study of Brassica—Leptosphaeria interactions. The genomic positions of the R genes were defined through molecular mapping and analysis with transgenic L. maculans isolates was used to confirm the identity of the introgressed genes where possible. Using L. maculans isolates of contrasting avirulence gene (Avr) profiles, we preformed extensive differential pathology for phenotypic comparison of the ILs to other B. napus varieties, demonstrating the ILs can provide for the accurate assessment of Avr-R gene interactions by avoiding non-Avr dependant alterations to resistance responses which can occur in some commonly used B. napus varieties. Whole-genome SNP-based assessment allowed us to define the donor parent introgressions in each IL and provide a strong basis for comparative molecular dissection of the pathosystem.

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“…Among the detected extracellular proteins is RD21, a secreted protease reported to be involved in Arabidopsis resistance to Botrytis cinerea infection but not bacterial pathogens (Shindo et al, 2012). Several pathogens secrete inhibitor proteins to counteract RD21-like activities, which indicates that such proteases play important roles in plant resistance (Zhang et al, 2014; Misas-Villamil et al, 2016). Thus, the detection of RD21 supports the idea of defense regulation through MPK3/6 by increasing release of antimicrobial proteins into the extracellular milieu.…”

Section: Discussionmentioning

confidence: 99%

Stress-Related Mitogen-Activated Protein Kinases Stimulate the Accumulation of Small Molecules and Proteins in Arabidopsis thaliana Root Exudates

et al. 2017

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A delicate balance in cellular signaling is required for plants to respond to microorganisms or to changes in their environment. Mitogen-activated protein kinase (MAPK) cascades are one of the signaling modules that mediate transduction of extracellular microbial signals into appropriate cellular responses. Here, we employ a transgenic system that simulates activation of two pathogen/stress-responsive MAPKs to study release of metabolites and proteins into root exudates. The premise is based on our previous proteomics study that suggests upregulation of secretory processes in this transgenic system. An advantage of this experimental set-up is the direct focus on MAPK-regulated processes without the confounding complications of other signaling pathways activated by exposure to microbes or microbial molecules. Using non-targeted metabolomics and proteomics studies, we show that MAPK activation can indeed drive the appearance of dipeptides, defense-related metabolites and proteins in root apoplastic fluid. However, the relative levels of other compounds in the exudates were decreased. This points to a bidirectional control of metabolite and protein release into the apoplast. The putative roles for some of the identified apoplastic metabolites and proteins are discussed with respect to possible antimicrobial/defense or allelopathic properties. Overall, our findings demonstrate that sustained activation of MAPKs alters the composition of apoplastic root metabolites and proteins, presumably to influence the plant-microbe interactions in the rhizosphere. The reported metabolomics and proteomics data are available via Metabolights (Identifier: MTBLS441) and ProteomeXchange (Identifier: PXD006328), respectively.

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Papain‐like cysteine proteases as hubs in plant immunity

Cited by 148 publications

References 49 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

Single R Gene Introgression Lines for Accurate Dissection of the Brassica - Leptosphaeria Pathosystem

Stress-Related Mitogen-Activated Protein Kinases Stimulate the Accumulation of Small Molecules and Proteins in Arabidopsis thaliana Root Exudates

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