Downy mildew disease promotes the colonization of romaine lettuce by Escherichia coli O157:H7 and Salmonella enterica.

Ivan Simko,Yaguang Zhou,Maria T Brandl

doi:10.1186/s12866-015-0360-5

Ivan Simko, Yaguang Zhou + Show 1 more

Open Access

https://doi.org/10.1186/s12866-015-0360-5

Copy DOI

Abstract

BackgroundDowny mildew, a plant disease caused by the oomycete Bremia lactucae, is endemic in many lettuce-growing regions of the world. Invasion by plant pathogens may create new portals and opportunities for microbial colonization of plants. The occurrence of outbreaks of Escherichia coli O157:H7 (EcO157) and Salmonella enterica Typhimurium (S. Typhimurium) infections linked to lettuce prompted us to investigate the role of downy mildew in the colonization of romaine lettuce by these human pathogens under controlled laboratory conditions.ResultsWhereas both EcO157 and S. Typhimurium population sizes increased 102-fold on healthy leaf tissue under conditions of warm temperature and free water on the leaves, they increased by 105-fold in necrotic lesions caused by B. lactucae. Confocal microscopy of GFP-EcO157 in the necrotic tissue confirmed its massive population density and association with the oomycete hyphae. Multiplication of EcO157 in the diseased tissue was significantly lower in the RH08-0464 lettuce line, which has a high level of resistance to downy mildew than in the more susceptible cultivar Triple Threat. qRT-PCR quantification of expression of the plant basal immunity gene PR-1, revealed that this gene had greater transcriptional activity in line RH08-0464 than in cultivar Triple Threat, indicating that it may be one of the factors involved in the differential growth of the human pathogen in B. lactucae lesions between the two lettuce accessions. Additionally, downy mildew disease had a significant effect on the colonization of EcO157 at high relative humidity (RH 90-100%) and on its persistence at lower RH (65-75%). The latter conditions, which promoted overall dryness of the lettuce leaf surface, allowed for only 0.0011% and 0.0028% EcO157 cell survival in healthy and chlorotic tissue, respectively, whereas 1.58% of the cells survived in necrotic tissue.ConclusionsOur results indicate that downy mildew significantly alters the behavior of enteric pathogens in the lettuce phyllosphere and that breeding for resistance to B. lactucae may lower the increased risk of microbial contamination caused by this plant pathogen.

Highlights

Downy mildew, a plant disease caused by the oomycete Bremia lactucae, is endemic in many lettuce-growing regions of the world
We did not test for the possible asymptomatic presence of the oomycete in some of the visually healthy tissue that was used in our study, the disease symptoms clearly resulted in greater population densities of the enteric pathogens than the seemingly healthy tissue
Typhimurium in the lesions increased at least 105-fold over 42 h at warm temperature. This high carrying capacity of the diseased leaf tissue is likely due to the abundant nutrients made available by the oomycete degradation of plant cells and their contents

Summary

Introduction

A plant disease caused by the oomycete Bremia lactucae, is endemic in many lettuce-growing regions of the world. Multiplication of EcO157 in the diseased tissue was significantly lower in the RH08-0464 lettuce line, which has a high level of resistance to downy mildew than in the more susceptible cultivar Triple Threat. Downy mildew disease had a significant effect on the colonization of EcO157 at high relative humidity (RH 90-100%) and on its persistence at lower RH (65-75%). The latter conditions, which promoted overall dryness of the lettuce leaf surface, allowed for only 0.0011% and 0.0028% EcO157 cell survival in healthy and chlorotic tissue, respectively, whereas 1.58% of the cells survived in necrotic tissue. The incidence of the disease in the Salinas growing region of Coastal California generally increases in the autumn lettuce crop [12]

Methods

Results

Conclusion