AUG 14, 2015 12:18 PM PDT

An Emerging Field of Study: Human Pathogens on Plants

WRITTEN BY: Sarah Hertrich
The CDC estimates the incidence of foodborne illness attributed to fruit and vegetable consumption at three million cases in the U.S. annually. The means by which food crops become contaminated with foodborne pathogens as well as how these organisms persist within the phyllosphere and rhizosphere of these plants is a complex issue. Outbreaks continue to occur with food crops and it is clear that different approaches must be taken in order to enhance the safety of these foods. Because of these reasons the fields of plant science and food safety have begin to merge in order to address the preharvest contamination issue in a new way.
By studying how plants respond to plant pathogens, we may understand how human pathogens interact with plants as well.
In general, many species of bacteria have close relationships with plants and in some cases promote plant growth and nitrogen uptake. Similar relationships exist with plant viruses; however, these relationships tend to be more detrimental to the plant when plant disease occurs along with large economic losses and threats to food security and public health. Alternatively, crops may become contaminated with bacterial and viral pathogens that are a threat to human health but not necessarily to plant health. Research has shown that plants can become contaminated with human pathogens in the pre-harvest environment through a variety of outlets including soil, feces, irrigation water, or water used to apply pesticides and fertilizers, dust, insects, land-applied manures and biosolids and directly from wild or domestic animals. Leafy greens are considered a high-risk food crop because they have been epidemiologically linked to foodborne illness, they are commonly consumed in their raw state, where little or no processing takes place to reduce contaminants. Leafy greens are not all the same when it comes to potential contamination. For example, spinach forms a canopy that may serve as a trap for zoonotic pathogens due to protection from environmental stressors, such as UV, if the plants become contaminated. Outer leaves of lettuce plants may provide a reservoir for pathogens but this route of contamination may not lead to illness. Addressing safer ways to manage crop growth and harvest is essential to minimizing microbial contamination. In order to address these issues we must first develop a better understanding of how human pathogenic bacteria and viruses interact with plants.

It has been previously demonstrated that human pathogenic viruses, such as human norovirus, can be internalized into leafy greens through the roots and foliar surfaces of lettuce plants although it is not known how often this naturally occurs in the field and how internalization physically affects the plant. It is important to determine the type of relationships that human pathogens have with plants, whether they be symbiotic, endophytic or antagonistic. For example, it was suggested by Dr. Adam Schikora’s research group at the Institute of Phytopathology and Zoology in Hesse, Germany that human pathogenic Salmonella typhimurium infect and intracellularly proliferate within tissues of Arabidopsis thaliana through both the root and shoot of the plant. Salmonella infection also yielded disease symptoms in the plants including wilting, chlorosis and death of infected plant organs compared to non-inoculated controls. However; in these experiments Salmonella was infiltrated into plants, an event that does not occur in nature. Arabidopsis plants responded immunologically similarly to Salmonella as they would to the plant pathogen Pseudomonas syringae (DC3000) by induction of the mitogen activated protein kinase (MAPK) cascades as well as by enhanced expression of pathogenesis related (PR) genes. There are also studies demonstrating that bacteria normally pathogenic to humans and other mammals can induce immune response in plants including Salmonella enterica, Pseudomonas aeruginosa, Burkholderia cepacia, Erwinia spp., Staphylococcus aureus, E. coli O157:H7, and Listeria monocytogenes.
Plant stomata, which function in plant transpiration, may also serve as portals of entry for human pathogens.
Most of the studies described above have been performed on Arabidopsis thaliana, which according to the National Institutes of Health (NIH), is a small flowering plant that is widely used as a model organism in plant biology (NIH, 2015). Arabidopsis is a member of the mustard (Brassicaceae) family that includes crop plants such as cabbage, cauliflower and broccoli. It is an important plant for genetic and biological research of crop plants although it has no importance in agriculture itself.  Approximately 115 Mb of the 125 Mb genome has been sequenced and annotated and there are extensive genetic and physical maps available of all 5 chromosomes. The life cycle of A. thaliana is short compared to most crop plants (only about 6 weeks) and can easily be cultivated in small spaces such as the laboratory or within a biochamber. There are a number of genetic mutant lines and genomic resources available to the scientific community, making A. thaliana a good candidate for multinational research in academia, industry and government. Because of all the above listed reasons, it can also be concluded that Arabidopsis serves as a good model for studying human foodborne pathogen – plant interactions.
Because its entire genome has been sequenced, we can use Arabidopsis thaliana to learn how plants respond to human pathogens.
Studies of the interactions between plants and plant pathogens, including the plant immune response, have led to the development of control measures for many devastating plant diseases. Through the study of the way plants respond to and effectively fight off plant pathogens, scientists have been able to develop plant breeding programs for disease resistant varieties. Many of the current control and prevention strategies for human pathogens on plants are at the post-harvest level - once the pathogens have already come into contact with or possibly penetrated the plant tissues. Alternative intervention measures target prevention of the initial contamination event. For effective measures to be developed for pre-harvest interventions, a better understanding of the mechanisms by which human pathogens colonize plants as well as how and if the plants are able to recognize these pathogens is needed.

The mechanism by which the plant immune system operates is through the detection of conserved microbial components. The plant physiological responses to plant infection can be due to activation of the induced systemic resistance (ISR) or systemic acquired resistance pathway (SAR). The SAR pathway is induced if the pathogen is able to elicit a hypersensitive reaction (HR), which causes apoptosis in the plant in order to rid itself of the infectious agent. These events may enable the plant to become more resistant to future attacks by the pathogen. When a plant is invaded by a pathogen, one of two defense signaling pathways are activated: a salicylic acid (SA) dependent pathway or an SA-independent pathway involving jasmonic acid (JA) or ethylene (ET) signaling molecules. JA-dependent and ET-dependent plant defenses are generally activated by necrotrophic pathogens and chewing insects, whereas SA-dependent defenses are often triggered by biotrophic pathogens. JA and SA signaling usually act antagonistically, but synergism between these two molecules has also been observed. The interactions among SA-, JA- and ethylene-dependent pathways are extremely complex. For example, during an immune response of A. thaliana to plant pathogen P. syringae DC3000, activation of the JA- pathway has been observed to suppress the SA-pathway and reduce the plants general resistance to the pathogen P. syrinage, among which most plants use the SA-pathway. It is also hypothesized that some virulent strains of P. syringae take advantage of this antagonistic interaction in order to suppress the Arabidopsis defensive response.

In the pre-harvest environment there are many control and prevention strategies currently used by produce growers that help protect plants from infection by plant pathogens and pests that can cause damage to crops. There are other guidelines, including Good Agricultural Practices (GAPs), which provide information for growers on how to prevent their crops from becoming contaminated with human pathogens; however, addressing this issue is much more complex in that we do not know exactly how or why human pathogens interact with plants. It has been hypothesized that the ability for human pathogens to colonize edible plants may be an effective survival strategy that provides a direct route from its excretion in the environment back to its numerous herbivorous and omnivorous hosts. The implementation of the Food Safety Modernization Act (FSMA) in 2011 and introduction of the Produce Safety Rules will now require qualified growers to follow more stringent food safety practices that could increase the cost of food production and subsequently raise the cost of food. In addition, food trends including the organic and non-GMO campaigns have led to a decrease in the use of fertilizers previously used to reduce crop loss as well as higher food prices for these commodities.
Plant growth promoting bacteria (PGPR) can be used to boost plant immunity, protecting plants from pathogens and increasing crop yield.
It would be ideal, to innovate technologies that could reduce contamination of crops by plant and human pathogens simultaneously. One potential solution includes the use of plant growth promoting rhizobacteria (PGPR) which can act as plant “probiotics”. PGPR are considered part of the natural microflora of plants as well as important contributors to plant health through plant growth promotion or biological disease control. They are often used to induce suppressiveness of plant pathogens by altering the diversity of microorganisms in the rhizosphere. In most cases, biological control by PGPR results from bacterial production of metabolites that directly inhibit the pathogen such as antibiotics, hydrogen cyanide, iron-chelating siderophores, and cell-wall degrading enzymes. Plant growth promotion is considered an indirect mechanism of disease control as the time a plant is in a susceptible state is shortened, allowing for the plant to escape infection. Use of PGPR have also been used to reduce plant contamination by foliar pathogens where PGPR control involves induction of plant host defenses. Recent studies have demonstrated the ability of PGPR Bacillus Subtilis to induce stomatal closure in lettuce and spinach as well as reduce the persistence of L. monocytogenes on these plants. Through a series of interactions between the human pathogen, the plant and the PGPR, the plant recruits the PGPR by secretion of malic acid to form biofilms on the roots of the plants which induces plant defenses and ultimately somtata closure.

The study of human pathogens on plants has opened our minds to complicated interactions among bacteria, viruses, and plants. There is more to the survival of human pathogens on plant leaf surfaces and in the soil; much more that has yet to be uncovered. Future research in this area will generate fundamental information regarding the physical and molecular mechanisms that enable human pathogens to attach, internalize, grow and survive in and on fresh produce, specifically leafy greens. Additionally this work will generate information on how plants interact with foodborne pathogens and if these associations affect the attachment and fate of human pathogens on fresh produce. There are many knowledge gaps involving how plants respond to human pathogen contamination which is the number one cause of foodborne illness in the US, with a majority of illnesses involving leafy greens. Information concerning human pathogen persistence and survival will impact growing and irrigation practices. Information gained by studying the plant defense response in relation to colonization by human pathogens may also impact pre-harvest growing practices.

Sources: Nature, Microbes and Infection, Applied and Environmental Microbiology, Phytopathology, Science, CDC, Annual Reviews in Phytopathology, Cell, Trends in Plant Science, Annual Reviews in Food Science and Technology, Journal of Food Protection, FDA, PloS One, Molecular Plant-Microbe Interactions, International Journal of Food MicrobiologyFoodborne Pathogens and Disease, FEMS Microbiology Reviews, The Arabidopsis Book, Proceedings of the National Academy of Sciences, Australasian Plant Pathology, Plant Journal, Current Opinion in Plant Biology, Plant Physiology, Plant Pathology, Microbes and Environments, NIH, Environmental Microbiology, Emerging Infectious Diseases, Journal of Bacteriology, ISME Journal, Plant Cell, Virology, Computational Structure in Biotechnology, BMC Microbiology, Anaerobe, Plant Diseases, Planta.
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About the Author
Doctorate (PhD)
I am a postdoctoral researcher with interests in pre-harvest microbial food safety, nonthermal food processing technologies, zoonotic pathogens, and plant-microbe interactions. My current research projects involve the optimization of novel food processing technologies to reduce the number of foodborne pathogens on fresh produce. I am a food geek!
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