publication . Article . Research . 2014

Pseudomonas syringaeEvades Host Immunity by Degrading Flagellin Monomers with Alkaline Protease AprA

Pel, Michiel J. C.; van Dijken, Anja J. H.; Bardoel, Bart W.; Seidl, Michael F.; van der Ent, Sjoerd; van Strijp, Jos A. G.; Pieterse, Corné M. J.;
Open Access
  • Published: 01 Jul 2014 Journal: Molecular Plant-Microbe Interactions, volume 27, pages 603-610 (issn: 0894-0282, Copyright policy)
  • Publisher: Scientific Societies
  • Country: Netherlands
Abstract
Bacterial flagellin molecules are strong inducers of innate immune responses in both mammals and plants. The opportunistic pathogen Pseudomonas aeruginosa secretes an alkaline protease called AprA that degrades flagellin monomers. Here, we show that AprA is widespread among a wide variety of bacterial species. In addition, we investigated the role of AprA in virulence of the bacterial plant pathogen P. syringae pv. tomato DC3000. The AprA-deficient DC3000 ΔaprA knockout mutant was significantly less virulent on both tomato and Arabidopsis thaliana. Moreover, infiltration of A. thaliana Col-0 leaves with DC3000 ΔaprA evoked a significantly higher level of express...
Subjects
Medical Subject Headings: fungi
free text keywords: Agronomy and Crop Science, Physiology, General Medicine, Virulence, Innate immune system, Botany, Immune receptor, Pseudomonas aeruginosa, medicine.disease_cause, medicine, Arabidopsis thaliana, biology.organism_classification, biology, Microbiology, Flagellin, biology.protein, Pathogen, Pseudomonas syringae, Arabidopsis, Gene Expression Regulation, Bacterial, Gene Expression Regulation, Enzymologic, Lycopersicon esculentum, Plant Diseases, Serine Endopeptidases, Virulence Factors, Taverne, Pseudomonas, host immune evasion, plant immunity, flagellin, alkaline protease
Funded by
EC| PLANTIMMUSYS
Project
PLANTIMMUSYS
The Plant Immune System: a multidisciplinary approach to uncover how plants simultaneously deal with beneficial and parasitic organisms to maximize profits and protection
  • Funder: European Commission (EC)
  • Project Code: 269072
  • Funding stream: FP7 | SP2 | ERC
60 references, page 1 of 4

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.

Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., GómezGómez, L., Boller, T., Ausubel, F. M., and Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983.

Bardoel, B. W., and Van Strijp, J. A. G. 2011. Molecular battle between host and bacterium: Recognition in innate immunity. J. Mol. Recognit. 24:1077-1086.

Bardoel, B. W., Van der Ent, S., Pel, M. J. C., Tommassen, J., Pieterse, C. M. J., Van Kessel, K. P. M., and Van Strijp, J. A. G. 2011. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7:e1002206. [OpenAIRE]

Bardoel, B. W., Van Kessel, K. P. M., Van Strijp, J. A. G., and Milder, F. J. 2012. Inhibition of Pseudomonas aeruginosa virulence: Characterization of the AprA-AprI interface and species selectivity. J. Mol. Biol. 415:573-583.

Bethesda Research Laboratories. 1986. BRL pUC host: E. coli competent cells. Focus 8:9.

Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu. Rev. Plant Biol. 60:379-406.

Boller, T., and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.

Bolton, M. D., Van Esse, H. P., Vossen, J. H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., Van den Berg, G. C. M., Borras-Hidalgo, O., Dekker, H. L., De Koster, C. G., de Wit, P. J., Joosten, M. H., and Thomma, B. P. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136.

Boyer, H. M., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472. [OpenAIRE]

Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q. Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W.-L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186. [OpenAIRE]

Chevance, F. F. V., and Hughes, K. T. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465. [OpenAIRE]

Clough, S. J., and Bent, A. F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.

Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., and Scheible, W. R. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139:5-17. [OpenAIRE]

De Jonge, R., Van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., Van der Krol, S., Shibuya, N., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2010. Conserved fungal LysM effector Ecp6 prevents chitintriggered immunity in plants. Science 329:953-955.

60 references, page 1 of 4
Abstract
Bacterial flagellin molecules are strong inducers of innate immune responses in both mammals and plants. The opportunistic pathogen Pseudomonas aeruginosa secretes an alkaline protease called AprA that degrades flagellin monomers. Here, we show that AprA is widespread among a wide variety of bacterial species. In addition, we investigated the role of AprA in virulence of the bacterial plant pathogen P. syringae pv. tomato DC3000. The AprA-deficient DC3000 ΔaprA knockout mutant was significantly less virulent on both tomato and Arabidopsis thaliana. Moreover, infiltration of A. thaliana Col-0 leaves with DC3000 ΔaprA evoked a significantly higher level of express...
Subjects
Medical Subject Headings: fungi
free text keywords: Agronomy and Crop Science, Physiology, General Medicine, Virulence, Innate immune system, Botany, Immune receptor, Pseudomonas aeruginosa, medicine.disease_cause, medicine, Arabidopsis thaliana, biology.organism_classification, biology, Microbiology, Flagellin, biology.protein, Pathogen, Pseudomonas syringae, Arabidopsis, Gene Expression Regulation, Bacterial, Gene Expression Regulation, Enzymologic, Lycopersicon esculentum, Plant Diseases, Serine Endopeptidases, Virulence Factors, Taverne, Pseudomonas, host immune evasion, plant immunity, flagellin, alkaline protease
Funded by
EC| PLANTIMMUSYS
Project
PLANTIMMUSYS
The Plant Immune System: a multidisciplinary approach to uncover how plants simultaneously deal with beneficial and parasitic organisms to maximize profits and protection
  • Funder: European Commission (EC)
  • Project Code: 269072
  • Funding stream: FP7 | SP2 | ERC
60 references, page 1 of 4

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.

Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., GómezGómez, L., Boller, T., Ausubel, F. M., and Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983.

Bardoel, B. W., and Van Strijp, J. A. G. 2011. Molecular battle between host and bacterium: Recognition in innate immunity. J. Mol. Recognit. 24:1077-1086.

Bardoel, B. W., Van der Ent, S., Pel, M. J. C., Tommassen, J., Pieterse, C. M. J., Van Kessel, K. P. M., and Van Strijp, J. A. G. 2011. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7:e1002206. [OpenAIRE]

Bardoel, B. W., Van Kessel, K. P. M., Van Strijp, J. A. G., and Milder, F. J. 2012. Inhibition of Pseudomonas aeruginosa virulence: Characterization of the AprA-AprI interface and species selectivity. J. Mol. Biol. 415:573-583.

Bethesda Research Laboratories. 1986. BRL pUC host: E. coli competent cells. Focus 8:9.

Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu. Rev. Plant Biol. 60:379-406.

Boller, T., and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.

Bolton, M. D., Van Esse, H. P., Vossen, J. H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., Van den Berg, G. C. M., Borras-Hidalgo, O., Dekker, H. L., De Koster, C. G., de Wit, P. J., Joosten, M. H., and Thomma, B. P. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136.

Boyer, H. M., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472. [OpenAIRE]

Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q. Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W.-L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186. [OpenAIRE]

Chevance, F. F. V., and Hughes, K. T. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465. [OpenAIRE]

Clough, S. J., and Bent, A. F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.

Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., and Scheible, W. R. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139:5-17. [OpenAIRE]

De Jonge, R., Van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., Van der Krol, S., Shibuya, N., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2010. Conserved fungal LysM effector Ecp6 prevents chitintriggered immunity in plants. Science 329:953-955.

60 references, page 1 of 4
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