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. 2004 Jun 29;101(26):9927-32.
doi: 10.1073/pnas.0401601101. Epub 2004 Jun 21.

A Family of Conserved Bacterial Effectors Inhibits Salicylic Acid-Mediated Basal Immunity and Promotes Disease Necrosis in Plants

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Free PMC article

A Family of Conserved Bacterial Effectors Inhibits Salicylic Acid-Mediated Basal Immunity and Promotes Disease Necrosis in Plants

Sruti DebRoy et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Salicylic acid (SA)-mediated host immunity plays a central role in combating microbial pathogens in plants. Inactivation of SA-mediated immunity, therefore, would be a critical step in the evolution of a successful plant pathogen. It is known that mutations in conserved effector loci (CEL) in the plant pathogens Pseudomonas syringae (the Delta CEL mutation), Erwinia amylovora (the dspA/E mutation), and Pantoea stewartii subsp. stewartii (the wtsE mutation) exert particularly strong negative effects on bacterial virulence in their host plants by unknown mechanisms. We found that the loss of virulence in Delta CEL and dspA/E mutants was linked to their inability to suppress cell wall-based defenses and to cause normal disease necrosis in Arabidopsis and apple host plants. The Delta CEL mutant activated SA-dependent callose deposition in wild-type Arabidopsis but failed to elicit high levels of callose-associated defense in Arabidopsis plants blocked in SA accumulation or synthesis. This mutant also multiplied more aggressively in SA-deficient plants than in wild-type plants. The hopPtoM and avrE genes in the CEL of P. syringae were found to encode suppressors of this SA-dependent basal defense. The widespread conservation of the HopPtoM and AvrE families of effectors in various bacteria suggests that suppression of SA-dependent basal immunity and promotion of host cell death are important virulence strategies for bacterial infection of plants.

Figures

Fig. 1.
Fig. 1.
Responses of apple (cultivar Jonathan, Left) and Arabidopsis thaliana (ecotype Col-0 gl1, Right) to infiltration of high concentrations of bacteria suspensions (OD600 of 0.2). Apple leaves inoculated with WT E. amylovora (Ea) showed disease necrosis (brown color) 17-18 h after inoculation, whereas apple leaves inoculated with the dspA/E mutant did not show any necrosis in two experiments and a delayed, very spotty necrosis at 24 h in one experiment. Arabidopsis leaves inoculated with DC3000 collapsed (shrunken appearance in this picture) 22-24 h after inoculation, whereas Arabidopsis leaves inoculated with the ΔCEL mutant showed delayed disease necrosis at 28-30 h after inoculation. Pictures were taken at 24 h after inoculation.
Fig. 2.
Fig. 2.
Enhanced growth of the ΔCEL mutant in SA-impaired plants. (A) DC3000 growth in Col-0 (black bars) and NahG (light gray bars) plants. ΔCEL mutant growth in Col-0 (dark gray bars) and NahG (white bars) plants. cfu, Colony-forming units. (B) DC3000 growth in WT (black bars) and eds5 (light gray bars) plants. ΔCEL mutant growth in WT (dark gray bars) and eds5 (white bars) plants. (C) Disease symptoms of Col-0 and NahG leaves infected by DC3000 or the ΔCEL mutant (OD600 = 0.002). Arrows indicate inoculated leaves.
Fig. 3.
Fig. 3.
Callose deposition in Arabidopsis and apple leaves. (A) Portions of Arabidopsis Col-0 gl1 leaves stained for callose deposits (white dots in these images) after inoculation with WT DC3000 or the ΔCEL mutant. (B) Portions of WT apple leaves stained to show callose deposition after inoculation with WT Erwinia amylovora (Ea) or the dspA/E mutant. Below leaf images, average numbers of callose deposits per field of view (0.9 mm2) are displayed with standard deviations as errors. (Scale bar, 100 μm.)
Fig. 4.
Fig. 4.
Callose deposition in Arabidopsis leaves. (A-C) Portions of Arabidopsis Col-0 and NahG leaves stained to show callose deposition after inoculation with the hrpA mutant (A), the ΔCEL mutant (B), and WT DC3000 (C). (D-F) Portions of Arabidopsis Col-0 and eds5 leaves stained for callose after inoculation with the hrpA mutant (D), the ΔCEL mutant (E), and WT DC3000 (F). (G and H) Average numbers of callose depositions per field of view (0.9 mm2) with standard deviations displayed as errors. (Scale bar, 100 μm.)
Fig. 5.
Fig. 5.
RNA gel blot analysis of PR-1 and PAD4 expression 3, 6, and 9 h after infiltration of 1 × 108 cfu/ml ΔCEL mutant (ΔCEL) and DC3000 (WT). Below each autoradiogram is a picture of the ethidium bromide-stained 28S ribosomal RNA.
Fig. 6.
Fig. 6.
Complementation of the ΔCEL mutant. (A) Bacterial populations in Col-0 gl1 plants inoculated with DC3000 (black bars), the ΔCEL mutant (white bars), and the ΔCEL mutant complemented with pORF43 (light gray bars). (B) Bacterial populations in young leaves of Col-0 gl1 plants inoculated with DC3000 (black bars), the ΔCEL mutant (white bars), and the ΔCEL mutant complemented with pEF (light gray bars). (C) Callose deposits in portions of Arabidopsis Col-0 gl1 leaves inoculated with DC3000, the ΔCEL mutant, and the ΔCEL mutant containing pORF43. (D) Average numbers of callose deposits per field of view with standard deviations displayed as errors. (E) Callose deposits in portions of Arabidopsis Col-0 gl1 leaves inoculated with DC3000, the ΔCEL mutant, and the ΔCEL mutant containing pEF. (F) Average numbers of callose deposits per field of view with standard deviations displayed as errors.
Fig. 7.
Fig. 7.
A hypothetical model for the activation and inactivation of cell wall-based basal immunity during Pst DC3000 infection of susceptible Arabidopsis. MAPK, mitogen-activated protein kinase; MAPKK, MAPK kinase; MAPKKK, MAPKK kinase.

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