Progress 01/01/16 to 12/31/20
Outputs
Target Audience:Results from this research were reported at the Food Research Institute's Annual meeting, an audience of researchers and industry representatives and to the scientific community at the Entomology Society of America's annual meeting, held virtually. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Dr. Barak supervised Dr. Kim Cowles and Victoria Harrod (Lason). How have the results been disseminated to communities of interest?Drs. Barak and Cowles and Victoria (Lason) Harrod have given talks at scientific conferences. Dr. Barak has given talks at research and government institutions. Dr. Barak and Victoria (Lason) Harrod have given talks and poster presentations to food industry representatives. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
We endeavored to uncover mechanisms that lead to persistence of S. enterica on plants infested with Hemipterans. Without the fundamental knowledge of how plant infestation by Hemipterans results in sustained populations of S. enterica, gains in food safety of raw produce is unlikely. Our investigations of Hemipterans with distinct feeding behaviors revealed that an intracellular style of feeding used by leafhopper with an auchenorrhynchan stylet cause more cellular damage than insects that use an intercellular penetration with a sternorrhynchans stylet such as an aphid. More cellular damage was correlated with higher S. enterica populations compared to healthy, undamaged plants. Interestingly, our expanded investigations with thrips revealed that cellular damage alone is not sufficient to result in higher S. enterica populations. When compared to water bombardment that caused more cellular damage, thrips infested plants had higher S. enterica populations with less cellular damage. These findings together suggest that mechanisms in addition to cellular damage by phytophagous insects are important for persistence of S. enterica on leaves of infested plants. In addition to the obvious or stealth cellular damage that phytophagous insects cause, they also alter plant hormones and hormone induced plant defenses. Leafhopper infestation activates the jasmonic acid (JA) defense response while S. enterica colonization triggered the salicylic acid (SA) response. We found that plants simultaneously colonized by S. enterica and infested with leafhoppers had both JA- and SA-inducible genes activated. Having somewhat opposing host defenses, one for herbivory and the other for biotrophic pathogens, may affect the crosstalk that occurs between the two antagonistic immune response pathways. As host defenses are being deployed, we measured S. enterica population distribution changes. At the single cell level, S. enterica prefers to colonize specific leaf surface niches, such as the base of glandular trichomes and at cell junctions. We found that in general, higher populations of S. enterica reside on the tips of tomato leaflets compared to the base or center third of the leaflet. However, following leafhopper infestation, we discovered higher S. enterica populations in the center third of the leaflet. Studies have been initiated to identify preferred leafhopper feeding sites across the leaf surface. We found that leafhoppers avoid leaf areas with S. enterica suggesting that the mechanism leading to S. enterica persistence and/or growth is not from direct interaction between insect and microbe. Furthermore, it is likely that a global response to both insect infestation and microbe colonization such as the mixed plant defense deployment results in higher S. enterica populations.
Publications
- Type:
Journal Articles
Status:
Accepted
Year Published:
2020
Citation:
Victoria Harrod, Russell L Groves, Matthew Maurice, and Jeri D. Barak. Frankliniella occidentalis facilitate Salmonella enterica survival in the phyllosphere. PLoSONE.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2020
Citation:
Lason, V., Groves, R., Barak, J. Frankliniella occidentalis facilitate Salmonella enterica survival in the phyllosphere. Entomological Society of America, November 11-25.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2020
Citation:
Victoria Harrod, Russell L Groves, Matthew Maurice, and Jeri D. Barak. Aster leafhoppers alter the natural distribution of Salmonella enterica in the tomato phyllosphere. Food Research Institute Annual Meeting, University of WI-Madison, May 19.
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Progress 01/01/19 to 12/31/19
Outputs
Target Audience:Results from this research were reported at the Food Research Institute's Annual meeting, an audience of researchers and industry representatives and to the scientific community at the Korean Rural Development Administration and attending the International Society-Molecular Plant - Microbe Interactions XVIII Congress satellite Meeting "Interactions between Plants and Human Pathogens held in Glasgow, Scotland and the Entomology Society of America's annual meeting, held in St. Louis. Changes/Problems:Initially, our research efforts this year were focused on studying the mechanisms responsible for persistence of S. enterica on Hemipteran (Aster leafhopper and green peach aphid) infested plants. However, a thrips-infestation of the basement plant growth chambers derailed these studies for several months, but opened a new avenue of inquiry that's described in the accomplishments. What opportunities for training and professional development has the project provided?Dr. Barak supervises Dr. Kim Cowles and mentors the PhD candidate, Victoria Harrod (Lason). Vicky attended two meetings where she discussed her research with both an audience of peer researchers and representatives from food companies interested in food safety. How have the results been disseminated to communities of interest?Dr. Barak has given three invited talks on the progress of this research, North Carolina State University, Rural Development Administration of Korea, and at the International Society-Molecular Plant - Microbe Interactions XVIII Congress. The PhD candidate supported by this project attended and presented their data at two scientific meetings. What do you plan to do during the next reporting period to accomplish the goals?During the next period, we will focus on the role of insect excrement, honeydew, in persistence of human pathogen populations on lettuce and tomato. We will examine honeydew as a nutrient source for human pathogen growth and its' role as plant defense modulator.
Impacts
What was accomplished under these goals?
We investigated S. enterica growth on plants infested with Hemipterans with distinct feeding behaviors, the Aster leafhopper has an intracellular style of penetration from an auchenorrhynchan stylet causes more cellular damage than intercellular penetration by a sternorrhynchans stylet, green peach aphid. Leafhopper infestation on S. enterica inoculated tomato plants resulted in higher solute leakage and significantly greater bacterial populations than plants absent of insects. While the highest populations of S. enterica are naturally found on the tips of tomato leaflets, leafhopper infestation altered the natural distribution of bacterial populations. In the presence of aphids, measurements of electrical conductivity were not significantly different between plants with or without insects. A complimentary experiment determined that increasing aphid populations, from one individual to three, did not alter the extent of solute leakage on tomato plants. These findings elucidate that cellular damage is only one of the many insect feeding behaviors of auchenorrhynchans which provide an enhanced environment for S. enterica proliferation. We expanded our study to include another common phytophageous insect. Thrips are a common pest of both lettuce and tomato, two key crops recently plagued with foodborne illness outbreaks of salmonellosis and gastroenteritis from Shiga-toxin producing E. coli. With a growth chamber full of thrips damaged plants and a robust thrips population, we used these plants for open arena studies to determine the fate of S. enterica introduced to plants post-insect infestation. S. enterica populations were higher in areas of thrips damage. One might assume this is of no importance, as consumers could avoid consuming thrips-damaged leaves, but in truth low levels of damage are not obvious and not likely to be avoided. A detailed investigation into how thrips alter the phyllosphere to the benefit of S. enterica, revealed that rasping, sucking damage to leaves is a part of the story, but not the whole story. Abiotic damage of the same magnitude caused by thrips feeding results in higher S. enterica populations, but not to the extent as those on plants with thrips infestation.
Publications
- Type:
Journal Articles
Status:
Submitted
Year Published:
2019
Citation:
Victoria Harrod, Russell L Groves, Matthew Maurice, and Jeri D. Barak. Frankliniella occidentalis facilitate Salmonella enterica survival in the phyllosphere. Appl. Environ. Microbiol.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2019
Citation:
Lason, V., Groves, R., Barak, J. Intracellular penetration by Macrosteles quadrilineatus enhances Salmonella enterica persistence in the phyllosphere. Entomological Society of America, St. Louis, Missouri, November 17 - 20.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2019
Citation:
Maurice, M., Lason, V., Barak, J., Groves, R. Cellular damage caused by Frankliniella occidentalis feeding increases Salmonella enterica persistence on tomato plants. Food Research Institute Annual Meeting, University of WI-Madison, May 23-24.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2019
Citation:
Lason, V., Maurice, M., Barak, J., Groves, R. How do leafhoppers enhance Salmonella enterica populations in the phyllosphere? Food Research Institute Annual Meeting, University of WI-Madison, May 23-24.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2019
Citation:
Jeri D. Barak. Different insects, different benefits from phytophagous insects for Salmonella enterica, IS-MPMI XVIII Congress satellite Meeting Interactions between Plants and Human Pathogens., Glasgow, Scotland.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2019
Citation:
Jeri D. Barak. Biomultipliers in plants that increase Salmonella enterica, Rural Development Administration, Jeonju, Korea, December 18.
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Progress 01/01/18 to 12/31/18
Outputs
Target Audience:Results from this research were reported at the Food Research Institute's annual meeting, an audience of researchers and industry representatives and to the scientific communitiesattending the International Society for Microbial Ecology in Leipzig, Germany and the Entomology Society of America's annual and central branch meetings, held in Vancouver, Canada and Madison, WI, respectively. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Dr. Barak supervises Dr. Kim Cowles, who in turn also supervises undergraduate researcher, Brett Plagenz. How have the results been disseminated to communities of interest?Dr. Barak has given two invited talks on the progress of this research. What do you plan to do during the next reporting period to accomplish the goals?We plan to initiate studies to determine the role of insect honeydew in Salmonella survival on leaves (objective 1), investigate the role of flagella and other microbial-associated molecular patterns in the tri-trophic interaction (objective 2), and complement mutants identified with defects in insect persistence or colonization (objective 3).
Impacts
What was accomplished under these goals?
We tested the hypothesis that infestation with leafhoppers alters the plant immune response and increases S. enterica persistence. We found that Salmonella populations persist at higher levels on tomato leaves infested with leaf hoppers. Leafhopper infestation activated the jasmonic acid (JA) defense response while S. enterica colonization triggered the salicylic acid (SA) response. In tomato plants co-treated with S. enterica and leafhoppers, both JA- and SA-inducible genes were activated, suggesting that the presence of leafhoppers may affect the crosstalk that occurs between the two antagonistic immune response pathways. To rule out the possibility that leafhoppers provide additional benefits to S. enterica, plants were treated with a chemical JA analog to activate the immune response in the absence of leafhoppers. Although bacterial populations continue to decline over time, analog treatment significantly increased bacterial persistence on the leaf surface. Bacterial mutant analysis determined that the bacterial flagellum, whether functional or not, was required for increased S. enterica survival after analog treatment. Further, we define a potential mechanism by which phytophagous insects enhance human enteric pathogen survival on leaves. Our data suggest that leafhopper-induced activation of the JA response in conjunction with plant responses to flg22 benefit S. enterica survival while also providing evidence that suggests additional mechanisms may remain to be discovered.
Publications
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2018
Citation:
Victoria Lason, Matthew Maurice, Russell L Groves, and Jeri D. Barak. Areas of macroscopic damage caused by western flower thrips (Frankliniella occidentalis) exhibit greater cellular damage and promote Salmonella enterica populations. 2018 Entomology Society of America Annual Meeting, November 11-14, Vancouver, BC, Canada.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2018
Citation:
Jeri D. Barak. Plant ecology of foodborne pathogens, International Society for Microbial Ecology, ISME17, August 12-17, Leipzig, Germany.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2018
Citation:
Jeri D. Barak, Kimberly N. Cowles, and Russell L. Groves. Phytophagous Hemipteran-induced activation of the jasmonic acid response benefits Salmonella enterica in a flagellum-dependent manner. ISME17, August 12-17, Leipzig, Germany.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2018
Citation:
Victoria Lason, Matthew Maurice, Russell L. Groves, and Jeri D. Barak. Analyzing how insect mechanisms and plant architecture influence Salmonella enterica populations. 2018 Food Research Institute Annual Meeting, May 23-24, Madison, WI
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2018
Citation:
Victoria Lason, Russell L. Groves, and Jeri D. Barak. Connecting insects and human enteric bacterial pathogens: using electrical conductivity as a proxy for direct plant damage caused by Macrosteles quadrilineatus in lettuce and tomato. 2018 Entomology Society of America, North Central Branch Meeting, August 7-11, Madison, WI
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Kimberly N. Cowles, Russell L. Groves, and Jeri D. Barak. Insect herbivory modulates plant immune responses to the benefit of Salmonella enterica. Front Microbiol. doi: 10.3389/fmicb.2018.01987
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Progress 01/01/17 to 12/31/17
Outputs
Target Audience:Results from this research were reported at the International Association of Food Protection's Annual meeting to an audience of researchers and industry representatives and to the scientific community attending the Molecular Genetics of Bacteria and Phage Meeting held at University of WI-Madison. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Dr. Barak supervises Dr. Kim Cowles who works on Objective 2, who in turn also supervises undergraduate researchers, Louise Pitcher and Brett Plagenz. Dr. Cowles attended the Molecular Genetics of Bacteria and Phage Meeting held at University of WI-Madison. How have the results been disseminated to communities of interest?Dr. Barak has given one invited talk on the progress of this research and Dr. Cowles presented a poster. What do you plan to do during the next reporting period to accomplish the goals?We plan to initiate studies to determine the role of insect honeydew in Salmonella survival on leaves (objective 1), investigate the role of flagella and other microbial-associated molecular patterns in the tri-trophic interaction (objective 2), and complement mutants identified with defects in insect persistence or colonization (objective 3).
Impacts
What was accomplished under these goals?
Under objective 1, we examined mechanisms that can influence Salmonella population dynamics on leaves and what role insect behavior plays. First, we mapped the distribution of Salmonella following dip-inoculations which mimic rain or contaminated irrigation water dispersal of the pathogen onto the leaf surface. We found that plant architecture did not influence the overall dispersal of Salmonella and that in general, gravitational forces on the water drops may be important. We investigated whether Salmonella dispersal was influenced by electrolyte leakage. Electrolyte leakage of healthy plants in the absence of insect infestation fails to explain Salmonella distribution on the leaf surface. Under objective 2, we conducted experiments to characterize plant defense changes due to insect feeding and their impact on Salmonella populations. The co-association of phytophagous insects, such as the Aster leafhopper, Macrosteles quadrilineatus, results in S. enterica populations that persist at higher levels for longer periods of time when compared to plants treated with S. enterica alone. We hypothesized that leafhoppers increase S. enterica persistence by altering the plant defense response to the benefit of the bacteria. Leafhopper infestation activated the jasmonic acid (JA) defense response while S. enterica colonization triggered the salicylic acid (SA) response. In tomato plants co-treated with S. enterica and leafhoppers, both JA- and SA-inducible genes were activated, suggesting that the presence of leafhoppers may affect the crosstalk that occurs between the two antagonistic immune response pathways. To rule out the possibility that leafhoppers provide additional benefits to S. enterica, plants were treated with chemical analogs of JA or SA to activate each immune response in the absence of leafhoppers. Although bacterial populations continue to decline over time, analog treatment significantly increased bacterial persistence on the leaf surface. Under objective 3, to characterize Salmonella mechanisms used during Hemipteran transmission to plant, we have screened a mutant library with 20,000 members to identify mutants with defects in insect persistence or colonization. Using the results from the library screen, we have focused our efforts on genes important for biofilm formation. We have screened mutants defective in curli and cellulose production for a role in insect colonization.
Publications
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2017
Citation:
How phytopathogens contribute to human pathogen survival on plants, International Association of Food Protectionist, St. Louis, MO
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2017
Citation:
Kimberly N Cowles, Russell L Groves, and Jeri D Barak. 2017. Phytophagous Insects Alter the Plant Immune Response and Contribute to an Increased Persistence of Salmonella enterica on Tomato Leaves. Molecular Genetics of Bacteria and Phage Meeting held at University of WI-Madison.
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Progress 01/01/16 to 12/31/16
Outputs
Target Audience:The target audiences for this period were plant scientists and produce producers. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Dr. Barak and co-PI, Dr. Groves, actively mentor Ryan Bower, who works on Objective 3. How have the results been disseminated to communities of interest?Dr. Barak has given two invited international talks on the progress of this research. What do you plan to do during the next reporting period to accomplish the goals?We plan to initiate studies to characterize insect factors that influence the survival and dispersal of human bacterial pathogens in and among plants and insect (objective 1), continue our investigation of plant defense changes (objective 2), and complement mutants identified with defects in insect persistence or colonization (objective 3).
Impacts
What was accomplished under these goals?
Under objective 2, we conducted experiments to characterize plant defense changes due to insect feeding and their impact on human bacterial pathogens causing illness through consumption of fresh produce. We have optimized RNA extraction and processing protocols to monitor tomato defense gene expression in response to the presence of Salmonella and phytophagous insects (leaf hoppers) and exogenous application of methyl jasmonate to stimulate the JA immune response in tomato leaves. We have demonstrated that leaf hoppers increase the persistence of Salmonella on tomato leaves. Our results indicate that the tomato JA immune response is differentially regulated in the presence of leaf hoppers, Salmonella, or leaf hoppers with Salmonella. Under objective 3, to characterize Salmonella mechanisms used during Hemipteran transmission to plant, we have screened a mutant library with 20,000 members to identify mutants with defects in insect persistence or colonization.
Publications
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2016
Citation:
Non-traditional partnerships: Salmonella enterica interactions with phytophagous insects. 2016. International Symposium Salmonella and Salmonellosis, Saint-Malo, France, June 6-8.
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2016
Citation:
Phytophagous Hemipterans as risk factors for leafy green contamination by Salmonella. 2016. Korean Society of Food Hygiene and Safety, Seoul, Korea, October 17.
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