Abstract
In contrast to many mammalian pathogens, potential bacterial pathogens of plants remain outside the host cell. The plant must, therefore, promote an active resistance mechanism to combat the extracellular infection. How this resistance against bacteria is manifested and whether similar processes mediate basal, gene-for-gene, and salicylate-associated defense, however, are poorly understood. Here, we identify a specific plasma membrane syntaxin, NbSYP132, as a component contributing to gene-for-gene resistance in Nicotiana benthamiana. Silencing NbSYP132 but not NbSYP121, the apparent orthologue of a syntaxin required for resistance to powdery mildew fungus, compromised AvrPto-Pto resistance. Because syntaxins may play a role in secretion of proteins to the extracellular space, we performed a limited proteomic analysis of the apoplastic fluid. We found that NbSYP132-silenced plants were impaired in the accumulation of at least a subset of pathogenesis-related (PR) proteins in the cell wall. These results were confirmed by both immunoblot analysis and imunolocalization of a PR protein, PR1a. These results implicate NbSYP132 as the cognate target soluble N-ethylmaleimide-sensitive factor attachment protein receptor for exocytosis of vesicles containing antimicrobial PR proteins. NbSYP132 also contributes to basal and salicylate-associated defense, indicating that SYP132-dependent secretion is a component of multiple forms of defense against bacterial pathogens in plants.
MeSH Terms
Gene Silencing
Molecular Sequence Data
Plant Diseases/genetics,microbiology
Plant Leaves/microbiology
Plant Proteins/antagonists & inhibitors,metabolism
Pseudomonas syringae/pathogenicity
Qa-SNARE Proteins/antagonists & inhibitors,genetics,physiology
Tobacco/metabolism,microbiology,physiology
Chemicals
Plant Proteins
Qa-SNARE Proteins
pathogenesis-related proteins, plant
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kalde Monika
Sainsbury Laboratory, Colney Lane, Norwich, Norfolk NR4 7UH, United Kingdom.
Nühse Thomas S
Findlay Kim
Peck Scott C
References (28)
28 references, click to expand
-
Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions.
Plant Cell. 2001 Mar;13(3):659-66
PMID: 11251103
-
Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells.
Cell Struct Funct. 2004 Apr;29(2):49-65
PMID: 15342965
-
Systemic acquired resistance.
Annu Rev Phytopathol. 2004;42:185-209
PMID: 15283665
-
Induction of protein secretory pathway is required for systemic acquired resistance.
Science. 2005 May 13;308(5724):1036-40
PMID: 15890886
-
Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato.
Annu Rev Phytopathol. 2003;41:215-43
PMID: 14527329
-
High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance.
EMBO J. 2003 Nov 3;22(21):5690-9
PMID: 14592968
-
The Rx gene from potato controls separate virus resistance and cell death responses.
Plant Cell. 1999 May;11(5):781-92
PMID: 10330465
-
SNARE protein structure and function.
Annu Rev Cell Dev Biol. 2003;19:493-517
PMID: 14570579
-
The DeltafliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells.
Mol Genet Genomics. 2003 Apr;269(1):21-30
PMID: 12715150
-
Synthesis of pathogenesis-related proteins in tobacco is regulated at the level of mRNA accumulation and occurs on membrane-bound polysomes.
Proc Natl Acad Sci U S A. 1985 Dec;82(23):7999-8003
PMID: 16593627
-
An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus.
Plant J. 2002 Mar;29(5):569-79
PMID: 11874570
-
Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain.
Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3135-40
PMID: 15703292
-
Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana.
Plant J. 2007 Feb;49(4):607-18
PMID: 17217460
-
A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana.
Plant J. 1999 May;18(3):277-84
PMID: 10377993
-
Common and contrasting themes of plant and animal diseases.
Science. 2001 Jun 22;292(5525):2285-9
PMID: 11423652
-
Plant pathogens and integrated defence responses to infection.
Nature. 2001 Jun 14;411(6839):826-33
PMID: 11459065
-
Decoding the patterns of self and nonself by the innate immune system.
Science. 2002 Apr 12;296(5566):298-300
PMID: 11951031
-
Bacterial disease resistance in Arabidopsis through flagellin perception.
Nature. 2004 Apr 15;428(6984):764-7
PMID: 15085136
-
A bacterial virulence protein suppresses host innate immunity to cause plant disease.
Science. 2006 Jul 14;313(5784):220-3
PMID: 16840699
-
The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae.
Mol Biol Cell. 2004 Nov;15(11):5118-29
PMID: 15342780
-
Host-microbe interactions: shaping the evolution of the plant immune response.
Cell. 2006 Feb 24;124(4):803-14
PMID: 16497589
-
Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing.
Plant J. 2001 Jan;25(2):237-45
PMID: 11169199
-
FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.
Mol Cell. 2000 Jun;5(6):1003-11
PMID: 10911994
-
Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility.
Nat Immunol. 2003 Dec;4(12):1247-53
PMID: 14625549
-
A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants.
Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8577-82
PMID: 12817082
-
A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin.
J Biol Chem. 2003 Nov 14;278(46):45248-54
PMID: 12949074
-
Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity.
J Bacteriol. 2003 Nov;185(22):6658-65
PMID: 14594840
-
SNARE-protein-mediated disease resistance at the plant cell wall.
Nature. 2003 Oct 30;425(6961):973-7
PMID: 14586469