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, 80 (10), 3173-80

Xanthomonas Perforans Colonization Influences Salmonella Enterica in the Tomato Phyllosphere

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Xanthomonas Perforans Colonization Influences Salmonella Enterica in the Tomato Phyllosphere

Neha Potnis et al. Appl Environ Microbiol.

Abstract

Salmonella enterica rarely grows on healthy, undamaged plants, but its persistence is influenced by bacterial plant pathogens. The interactions between S. enterica, Xanthomonas perforans (a tomato bacterial spot pathogen), and tomato were characterized. We observed that virulent X. perforans, which establishes disease by suppressing pathogen-associated molecular pattern (PAMP)-triggered immunity that leads to effector-triggered susceptibility, created a conducive environment for persistence of S. enterica in the tomato phyllosphere, while activation of effector-triggered immunity by avirulent X. perforans resulted in a dramatic reduction in S. enterica populations. S. enterica populations persisted at ~10 times higher levels in leaves coinoculated with virulent X. perforans than in those where S. enterica was applied alone. In contrast, S. enterica populations were ~5 times smaller in leaves coinoculated with avirulent X. perforans than in leaves inoculated with S. enterica alone. Coinoculation with virulent X. perforans increased S. enterica aggregate formation; however, S. enterica was not found in mixed aggregates with X. perforans. Increased aggregate formation by S. enterica may serve as the mechanism of persistence on leaves cocolonized by virulent X. perforans. S. enterica association with stomata was altered by X. perforans; however, it did not result in appreciable populations of S. enterica in the apoplast even in the presence of large virulent X. perforans populations. Gene-for-gene resistance against X. perforans successively restricted S. enterica populations. Given the effect of this interaction, breeding for disease-resistant cultivars may be an effective strategy to limit both plant disease and S. enterica populations and, consequently, human illness.

Figures

FIG 1
FIG 1
S. enterica and X. perforans population dynamics on tomato plants. S. enterica (A) and X. perforans (B) populations (log CFU/cm2) on tomato leaves were sampled every 2 days for 14 days postinoculation (dpi). Plants were inoculated with S. enterica and virulent X. perforans (asterisks and dotted lines), S. enterica and avirulent X. perforans (open circles and solid lines), or S. enterica alone (solid circles and dashed lines). The data represent two independent experiments combined, since no significant difference existed among experimental replicates (experiment:dpi:treatment; P = 0.1 [S. enterica] and P = 0.6 [X. perforans]). The lines correspond to a linear regression model and the shaded areas to their associated 95% confidence intervals.
FIG 2
FIG 2
Effect of leaf age on S. enterica and X. perforans population dynamics on tomato plants. Shown is separation of the data in Fig. 1 by leaf age. S. enterica (A) and X. perforans (B) populations (log CFU/cm2) on tomato leaves were sampled every 2 days for 14 days postinoculation (dpi). Plants were inoculated with S. enterica and virulent X. perforans (asterisks and dotted lines), S. enterica and avirulent X. perforans (open circles and solid lines), or S. enterica alone (solid circles and dashed lines). The data represent two independent experiments combined, since no significant difference existed among experimental replicates (experiment:dpi:treatment:age; P = 0.1 [S. enterica] and P = 0.5 [X. perforans]). The lines correspond to a linear regression model and the shaded areas to their associated 95% confidence intervals.
FIG 3
FIG 3
S. enterica populations are influenced by pathogenicity of X. perforans. S. enterica (A) and X. perforans (B) populations (log CFU/cm2) on tomato leaves were sampled every 2 days for 14 days postinoculation (dpi). Plants were inoculated with S. enterica and virulent X. perforans (106 CFU/ml, asterisks and dotted lines; 105 CFU/ml, triangles and long-dashed lines), S. enterica and avirulent X. perforans (open circles and solid lines), or S. enterica alone (solid circles and short-dashed line). The data represent two independent experiments combined, since no significant difference existed among experimental replicates (experiment:dpi:treatment; P = 0.5 [S. enterica] and P = 0.1 [X. perforans]). The lines correspond to a linear regression model and the shaded areas to their associated 95% confidence intervals.
FIG 4
FIG 4
S. enterica and virulent X. perforans tomato leaf colonization. Plants were inoculated with S. enterica and virulent X. perforans, S. enterica and avirulent X. perforans, or S. enterica alone, and middle leaves were sampled for confocal microscopy 7 days postinoculation. Shown is a representative overlapping z-stack from confocal scanning laser microscopy of a middle leaf from a plant inoculated with S. enterica and virulent X. perforans (z-stack spanning 27-μm depth at ×40 magnification). S. enterica cells appear blue, and X. perforans appears green. Scale bar = 25 μm.
FIG 5
FIG 5
S. enterica colonization of stomata in the presence of X. perforans. Plants were inoculated with S. enterica and virulent X. perforans, S. enterica and avirulent X. perforans, or S. enterica alone, and middle leaves were sampled for confocal microscopy at 2 days postinoculation (dpi) and 7 dpi. Shown is a representative confocal laser scanning micrograph of a middle leaf from a plant inoculated with S. enterica and virulent X. perforans sampled at 7 dpi. S. enterica cells appear blue, and X. perforans appears green. Magnification, ×40. Scale bar = 25 μm.
FIG 6
FIG 6
S. enterica association with stomata in the presence of X. perforans is independent of phytobacterial pathogenicity. Plants were inoculated with S. enterica and virulent X. perforans (vXp), S. enterica and avirulent X. perforans (avirXp), or S. enterica alone (No Xp), and middle leaves were sampled for confocal microscopy at 2 days postinoculation and 7 dpi. Stomata from 10 random fields of view per leaf at ×40 magnification were examined for the presence of S. enterica from one leaf taken from each of three plants. The experiment was repeated at least three times. Average percentages of stomata colonized by S. enterica are shown for 2 dpi (white bars) and 7 dpi (gray bars). The error bars indicate standard deviations.

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