Human Pathogens on Plants: Designing a Multidisciplinary Strategy for Research

Oklahoma State University, Entomology and Plant Pathology, 127 Noble Research Center, Stillwater, Oklahoma, United States, 74078, 405-744-9948, 405-744-6039
Phytopathology (Impact Factor: 3.12). 02/2013; 103(4). DOI: 10.1094/PHYTO-09-12-0236-IA
Source: PubMed


Recent efforts to address concerns about microbial contamination of food plants and resulting foodborne illness have prompted new collaboration and interactions between the scientific communities of plant pathology and food safety. This article provides perspectives from scientists of both disciplines, and presents selected research results and concepts that highlight existing and possible future synergisms for audiences of both disciplines. Plant pathology is a complex discipline that encompasses studies of the dissemination, colonization and infection of plants by microbes such as bacteria, viruses, fungi and oomycetes. Plant pathologists study plant diseases as well as host plant defense responses and disease management strategies with the goal of minimizing disease occurrences and impacts. Repeated outbreaks of human illness attributed to the contamination of fresh produce, nuts and seeds, and other plant-derived foods by human enteric pathogens such as Shiga toxin-producing Escherichia coli and Salmonella spp. have led some plant pathologists to broaden the application of their science in the past two decades, to address problems of human pathogens on plants (HPOPs). Food microbiology, which began with the study of microbes that spoil foods and those that are critical to produce food, now also focuses study on how foods become contaminated with pathogens and how this can be controlled or prevented. Thus, at the same time, public health researchers and food microbiologists have become more concerned about plant-microbe interactions before and after harvest. New collaborations are forming between members of the plant pathology and food safety of their science to address problems of human pathogens on plants (HPOPs). New interactions and collaborations are forming between members of the plant pathology and food safety communities, leading to enhanced research capacity and greater understanding of the issues for which research is needed. The two communities use somewhat different vocabularies and conceptual models. For example, traditional plant pathology concepts such as the disease triangle and the disease cycle can help to define cross-over issues that pertain also to HPOP research, and can suggest logical strategies for minimizing the risk of microbial contamination. Continued interactions and communication among these two disciplinary communities is essential, and can be achieved by the creation of an interdisciplinary Research Coordination Network. We hope that this article, an introduction to the multidisciplinary HPOP arena, will be useful to researchers in many related fields.

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Available from: Jacqueline Fletcher, Mar 19, 2015
    • "Leafy vegetables, which are often consumed raw, can be involved in foodborne illness outbreaks linked to enteric human pathogens including Escherichia coli O157:H7, Listeria monocytogenes and Salmonella spp. Contamination can occur by food handlers in food service establishments or by farm-derived pollution, where animals are considered the primary source of contamination (Berger et al., 2010; Fletcher et al., 2013; Franz et al., 2007; Park et al., 2012). In the past few years, some foodborne disease outbreaks associated with fresh produce contaminated with these three pathogens have been reported in several countries, underlying a significant increase of vegetables as vehicles of foodborne organisms' transmission (DeWaal and Bhuiya, 2007; Holden et al., 2009). "
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    ABSTRACT: Outbreaks of foodborne illness, resulting from the consumption of fresh produce contaminated with human pathogens, are increasing. Potential uptake and persistence of human pathogens within edible parts of consumed fresh vegetables become an important issue in food safety. This study was conducted to assess the potential uptake and internalization of Escherichia coli O157:H7 and Listeria monocytogenes from an autoclaved substrate into edible parts of basil and baby salad plants (lettuce, cultivated rocket, wild rocket and corn salad) from 20 to 60–80 days after inoculation, when plants are ready to be harvested and commercialized. Plants were grown in mesocosms under different temperature conditions (24 °C and 30 °C) and the growing substrate was inoculated using contaminated irrigation water (7 log CFU/mL). E. coli O157:H7 could be internalized in the leaves of the tested leafy vegetables through the roots and persist up to the harvesting time with negligible differences between 24 °C and 30 °C. Significant decreases in pathogen titers were observed over time in the growing substrate on which the plants grew, until the last sampling time. In contrast, L. monocytogenes internalized and persisted only in lettuce mesocosms at 24 °C. Neither pathogen was observed in basil leaves. Similarly, in basil growing substrates, enteric bacteria were undetectable at the end of the experiments, suggesting that basil plants may produce and release antimicrobial compounds active against both bacteria in root exudates. These results suggest that enteric bacteria are able to persist within baby salad leaves up to market representing a risk for consumer's health.
    No preview · Article · Oct 2014 · International Journal of Food Microbiology
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    • "Several reports have demonstrated that certain human pathogens can colonize plants both at pre- and post-harvest stages, which is the cause of various outbreaks of foodborne human illnesses (Fletcher et al., 2013). These findings have expanded the research interest on so-called human pathogens on plants (HPOPs) as a means to explore and develop new avenues to increase food safety. "
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    ABSTRACT: Infections with Salmonella enterica belong to the most prominent causes of food poisoning and infected fruits and vegetables represent important vectors for salmonellosis. Although it was shown that plants raise defense responses against Salmonella, these bacteria persist and proliferate in various plant tissues. Recent reports shed light into the molecular interaction between plants and Salmonella, highlighting the defense pathways induced and the means used by the bacteria to escape the plant immune system and accomplish colonization. It was recently shown that plants detect Salmonella pathogen-associated molecular patterns (PAMPs), such as the flagellin peptide flg22, and activate hallmarks of the defense program known as PAMP-triggered immunity (PTI). Interestingly, certain Salmonella strains carry mutations in the flg22 domain triggering PTI, suggesting that a strategy of Salmonella is to escape plant detection by mutating PAMP motifs. Another strategy may rely on the type III secretion system (T3SS) as T3SS mutants were found to induce stronger plant defense responses than wild type bacteria. Although Salmonella effector delivery into plant cells has not been shown, expression of Salmonella effectors in plant tissues shows that these bacteria also possess powerful means to manipulate the plant immune system. Altogether, these data suggest that Salmonella triggers PTI in plants and evolved strategies to avoid or subvert plant immunity.
    Full-text · Article · Apr 2014 · Frontiers in Microbiology
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    • "The frequency and severity of produce-related foodborne illness outbreaks have increased in the last few decades [1,2]. Although consumption of fruits and vegetables has risen in recent years, these well-publicized foodborne outbreaks trigger consumer concerns about the safety of fresh produce, and impose a negative impact on the agricultural sector. "
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    ABSTRACT: Recently, most foodborne illness outbreaks of salmonellosis have been caused by consumption of contaminated fresh produce. Yet, the mechanisms that allow the human pathogen Salmonella enterica to contaminate and grow in plant environments remain poorly described. We examined the effect of feeding by phytophagous insects on survival of S. enterica on lettuce. Larger S. enterica populations were found on leaves infested with Macrosteles quadrilineatus. In contrast, pathogen populations among plants exposed to Frankliniella occidentalis or Myzus persicae were similar to those without insects. However, on plants infested with F. occidentalis, areas of the infested leaf with feeding damage sustained higher S. enterica populations than areas without damage. The spatial distribution of S. enterica cells on leaves infested with F. occidentalis may be altered resulting in higher populations in feeding lesions or survival may be different across a leaf dependent on local damage. Results suggest the possibility of some specificity with select insects and the persistence of S. enterica. Additionally, we demonstrated the potential for phytophagous insects to become contaminated with S. enterica from contaminated plant material. S. enterica was detected in approximately 50% of all M. quadrilineatus, F. occidentalis, and M. persicae after 24 h exposure to contaminated leaves. Particularly, 17% of F. occidentalis, the smallest of the insects tested, harbored more than 10(2) CFU/F. occidentalis. Our results show that phytophagous insects may influence the population dynamics of S. enterica in agricultural crops. This study provides evidence of a human bacterial pathogen interacting with phytophagous insect during plant infestation.
    Full-text · Article · Oct 2013 · PLoS ONE
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