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, 103 (4), 326-32

Escherichia Coli O157:H7 Induces Stronger Plant Immunity Than Salmonella Enterica Typhimurium SL1344

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Escherichia Coli O157:H7 Induces Stronger Plant Immunity Than Salmonella Enterica Typhimurium SL1344

Debanjana Roy et al. Phytopathology.

Abstract

Consumption of fresh produce contaminated with bacterial human pathogens has resulted in various, sometimes deadly, disease outbreaks. In this study, we assessed plant defense responses induced by the fully pathogenic bacteria Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium SL1344 in both Arabidopsis thaliana and lettuce (Lactuca sativa). Unlike SL1344, O157:H7 induced strong plant immunity at both pre-invasion and post-invasion steps of infection. For instance, O157:H7 triggered stomatal closure even under high relative humidity, an environmental condition that generally weakens plant defenses against bacteria in the field and laboratory conditions. SL1344 instead induced a transient stomatal immunity. We also observed that PR1 gene expression was significantly higher in Arabidopsis leaves infected with O157:H7 compared with SL1344. These results suggest that plants may recognize and respond to some human pathogens more effectively than others. Furthermore, stomatal immunity can diminish the penetration of human pathogens through the leaf epidermis, resulting in low bacterial titers in the plant apoplast and suggesting that additional control measures can be employed to prevent food contamination. The understanding of how plant responses can diminish bacterial contamination is paramount in preventing outbreaks and improving the safety of food supplies.

Figures

Fig. 1
Fig. 1
Human pathogens induce unique stomatal movements. A, Arabidopsis and B, lettuce heads were incubated with O157:H7 or SL1344 under varying relative humidity (RH). Results are shown as mean of stomatal aperture width (n=50–70) ± SE. Statistical significance of the difference in the means (mock versus bacterium treatment) was detected with two-tailed Student’s t-test (*** = p<0.001). C, Hydroponically grown lettuce heads incubated at 60% or >95% RH. Roots of all plants were kept moist for the duration of the experiment.
Fig. 2
Fig. 2
High RH favors penetration and survival of SL1344, but not O157:H7. A and B, Arabidopsis and C, lettuce. Bacterial enumeration in the leaf apoplast at different days (d) after dip-inoculation with O157:H7 or SL1344 under varying relative humidity (RH). Results are shown as the mean (n=12) ± SE. Statistical significance of the difference in the means (60% versus >95% RH at each time point) was detected with two-tailed Student’s t-test (* = p<0.05, ** = p<0.01).
Fig. 3
Fig. 3
SL1344 cannot actively open stomata. Arabidopsis plants were dip-inoculated with SL1344 and maintained at 60% RH in the dark or under light for the duration of the experiment. Results are shown as mean of stomatal aperture width (n=50–70) ± SE. Statistical significance of the difference in the means (mock versus bacterium treatment at specific time points) was detected with two-tailed Student’s t-test (*** = p<0.001).
Fig. 4
Fig. 4
Strong PTI overrides the effect of high RH in opening stomata. Stomatal response to different concentration of flg22 under varying RH and constant light. Arabidopsis (A) or lettuce (B) leaves were floated on either water or flg22 solution and stomatal aperture was measured 4 h post incubation. Results are shown as mean of stomatal aperture width (n=50–70) ± SE. Statistical significance of the difference in the means (60% versus >95% RH) was detected with two-tailed Student’s t-test (*** = p<0.001).
Fig. 5
Fig. 5
Stomatal immunity reduces penetration of human pathogens through the leaf epidermis. ost1-2 and the wild type Landsberg erecta Ler) plants were dip-inoculated with O157:H7 or SL1344. A, The pictures show Ler and ost1-2 mutant plants kept at 60% RH for the duration of the experiments. Note that this moderate RH does not cause plants to wilt. B, Stomatal aperture width was measure 2 h after inoculation with bacteria or water control. Results are shown as mean of stomatal aperture width (n=50–70) ± SE. C, Bacterial enumeration in the leaf apoplast at different days (d) after inoculation. Results are shown as the mean (n=18) ± SE. Statistical significance of the difference in the means (Ler versus ost1-2) was detected with two-tailed Student’s t-test (** = p<0.01, *** = p<0.001).
Fig. 6
Fig. 6
O157:H7 induces higher level of PR1 gene expression than SL1344. Expression of PR1 gene (At2g14610) at 2 and 8 h post inoculation with bacteria relative to the mock control as determined by RT-qPCR. Statistical significance of the difference in the mean expression of PR1 in response to SL1344 and O157:H7 relative to that in the mock control was detected with two-tailed Student’s t-test (* = p<0.05, ** = p<0.01).

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