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Publication #SL414

Impact of Tomato Varieties and Maturity State on Susceptibility of Tomatoes to Salmonella1

Massimiliano Marvasi, George Hochmuth, and Max Teplitski2

From 1998 to 2007, fresh fruits, vegetables, spices, and nuts were commonly linked with outbreaks of human gastroenteritis (Batz, Hoffman, and Morris 2011). Non-typhoidal Salmonella has emerged as one of the problematic human pathogens associated with fresh produce, nuts, and complex foods containing them (Batz, Hoffman, and Morris 2011; DeWaal, Tian, and Plunkett 2009). This fact sheet was produced to provide up-to-date information about tomato production practices and their relationships with Salmonella. This information should be useful for county UF/IFAS Extension agents in their vegetable education programs.

Even though Salmonella has long been considered a zoonotic pathogen (i.e., communicable from animals to humans), it is clear that human salmonellosis is also likely to result from the consumption of plant-based (mostly raw) foods. Thus, it appears that Salmonella and pathogenic E. coli may persist on plants between encounters with their animal hosts as a part of their normal lifecycle. Recent research indicates that the outcomes of plant interactions with Salmonella and pathogenic E. coli to some extent depend on the plant host: colonization of plant tissues varied not only among plant species, but also among plant varieties (Jablasone, Warriner, and Griffiths 2005; Barak, Kramer, and Hao 2011; Klerks et al. 2007; Quilliam, Williams, and Jones 2012). This raises the intriguing possibility that cultivar selection could be used to identify crop varieties that may be less conducive to proliferation of human pathogens.

Figure 1. 

Tomatoes of different varieties at different maturity stages are cued for testing for their resistance to Salmonella


Credit:

Max Teplitski, UF/IFAS


[Click thumbnail to enlarge.]

Several recent studies compared the extent to which tomato genotype affects the colonization of plant tissues by Salmonella (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). Overall, none of the tested tomato varieties were completely “resistant” to Salmonella, although there were hundred fold differences in the population sizes of the pathogen on tomatoes and within fruit tissues (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). In a limited survey of tomato varieties, there were no detectable patterns in susceptibility of heirloom or commercial varieties/hybrids to Salmonella. However, cherry tomatoes were generally less conducive to proliferation of Salmonella (Marvasi, Noel, et al. 2014). Tomatoes carrying ripening mutations (rin [ripening-inhibitor], nor [nonripening], Nr [never-ripe]) were significantly less conducive to Salmonella proliferation (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). However, the biochemical basis of why these mutants are less susceptible to Salmonella is not yet known.

Significant differences in the Salmonella colonization of tomatoes at different maturity stages have been observed (Marvasi, Cox, et al. 2013; Shi et al. 2007) and are consistent with the observation that ripe fruits are generally more susceptible to opportunistic pathogens. Differences in proliferation of Salmonella in mature and immature tomatoes did not seem to depend on the pigmentation of the ripe fruit (e.g., red, yellow, pink, brown, or green). How well do these differences observed in the greenhouse correlate to the susceptibility of field-grown tomatoes to Salmonella? When four tomato varieties—Bonny Best, Florida 47, Sebring, and Solar Fire—were tested in the field, their levels of susceptibility to Salmonella did not closely correlate to those observed in the greenhouse studies (Marvasi, Noel, et al. 2014). What is responsible for these observed differences is not yet clear; however, crop production practices and diversity of the microbial communities associated with fruits are known to affect the outcomes of interactions between human pathogens and crops (Marvasi, Cox, et al. 2013; Gutierrez-Rodriguez et al. 2012; Lopez-Velasco et al. 2012; Poza-Carrion, Suslow, and Lindow 2013; Williams et al. 2013).

Under the field conditions and in greenhouse tests, ripe tomatoes supported more rapid proliferation of Salmonella than immature green tomatoes (Shi et al. 2007; Marvasi, George, et al. 2014; Marvasi, Hochmuth, et al. 2013). Final cell numbers of Salmonella were, on average, tenfold higher in ripe tomatoes compared to the unripe tomatoes under the same conditions. In each season, there were samples in which Salmonella populations within red ripe tomatoes increased by at least 105 from the initial dose of ~ 102 cells.

Conclusions

Once contaminated, red ripe tomatoes are significantly more conducive to proliferation of Salmonella than green or partially ripe tomatoes. Cherry tomatoes tend to be less conducive to proliferation of Salmonella, compared to larger-fruited tomatoes. Generally, susceptibility of tomatoes to Salmonella did not correlate with fruit color (yellow, ivory, brown, pink, red) or with whether a variety was heirloom or a modern commercial hybrid. However, levels that Salmonella reached in fruits of different varieties were tomato genotype–dependent. Under some field conditions, tomatoes carrying ripening-related mutations were less conducive to proliferation of Salmonella.

References

Barak, J. D., L. C. Kramer, and L. Y. Hao. 2011. “Colonization of tomato plants by Salmonella enterica is cultivar dependent, and type 1 trichomes are preferred colonization sites.” Appl Environ Microbiol 77: 498–504.

Batz, M. B., S. Hoffman, and J. G. Morris. 2011. Ranking the risks: the 10 pathogen-food combinations with the greatest burden on public health. Gainesville, FL: University of Florida, Emerging Pathogens Institute.

DeWaal, C. S., X. A. Tian, and D. Plunkett. 2009. Outbreak Alert! Center for Science in Public Interest.

Gutierrez-Rodriguez, E., A. Gundersen, A. O. Sbodio, and T. V. Suslow. 2012. “Variable agronomic practices, cultivar, strain source and initial contamination dose differentially affect survival of Escherichia coli on spinach.” J Appl Microbiol 112: 109–118.

Jablasone, J., K. Warriner, and M. Griffiths. 2005. “Interactions of Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocytogenes plants cultivated in a gnotobiotic system.” Int J Food Microbiol 99: 7–18.

Klerks, M. M., E. Franz, M. van Gent-Pelzer, C. Zijlstra, and A. H. van Bruggen. 2007. “Differential interaction of Salmonella enterica serovars with lettuce cultivars and plant-microbe factors influencing the colonization efficiency.” Isme J 1: 620–631.

Lopez-Velasco, G., A. Sbodio, A. Tomas-Callejas, P. Wei, K. H. Tan, et al. 2012. “Assessment of root uptake and systemic vine-transport of Salmonella enterica sv. Typhimurium by melon (Cucumis melo) during field production.” Int J Food Microbiol 158: 65–72.

Marvasi, M., C. E. Cox, Y. Xu, J. T. Noel, J. J. Giovannoni, et al. 2013. “Differential regulation of Salmonella typhimurium genes involved in O-antigen capsule production and their role in persistence within tomato fruit.” Mol Plant Microbe Interact 26: 793–800.

Marvasi, M., A. S. George, M. Giurcanu, G. J. Hochmuth, J. T. Noel, et al. 2014. “Effects of nitrogen and potassium fertilization on the susceptibility of tomatoes to post-harvest proliferation of Salmonella enterica.” Food Microbiol 43: 20–27.

Marvasi, M., G. J. Hochmuth, M. C. Giurcanu, A. S. George, J. T. Noel, et al. 2013. “Factors that affect proliferation of Salmonella in tomatoes post-harvest: the roles of seasonal effects, irrigation regime, crop and pathogen genotype.” PLoS One 8: e80871.

Marvasi, M., J. T. Noel, A. S. George, M. A. Farias, K. T. Jenkins, et al. 2014. “Ethylene signalling affects susceptibility of tomatoes to Salmonella.” Microb Biotechnol 7: 545–555.

Poza-Carrion, C., T. V. Suslow, and S. E. Lindow. 2013. “Resident bacteria on leaves enhance survival of immigrant cells of Salmonella enterica.” Phytopathology 103.

Quilliam, R. S., A. P. Williams, and D. L. Jones. 2012. “Lettuce cultivar mediates both phyllosphere and rhizosphere activity of Escherichia coli O157:H7.” PLoS One 7: e33842.

Shi, X., A. Namvar, M. Kostrzynska, R. Hora, and K. Warriner. 2007. “Persistence and growth of different Salmonella serovars on pre- and postharvest tomatoes.” J Food Prot 70: 2725–2731.

Williams, T. R., A. L. Moyne, L. J. Harris, and M. L. Marco. 2013. “Season, irrigation, leaf age, and Escherichia coli inoculation influence the bacterial diversity in the lettuce phyllosphere.” PLos One 8: e68642.

Footnotes

1.

This document is SL414, one of a series of the Soil and Water Science Department, UF/IFAS Extension. Original publication date December 2014. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

Massimiliano Marvasi, research assistant professor, Soil and Water Science Department; George Hochmuth, professor, Soil and Water Science Department; and Max Teplitski, associate professor, Soil and Water Science Department; UF/IFAS Extension, Gainesville, FL 32611.


The Institute of Food and Agricultural Sciences (IFAS) is an Equal Opportunity Institution authorized to provide research, educational information and other services only to individuals and institutions that function with non-discrimination with respect to race, creed, color, religion, age, disability, sex, sexual orientation, marital status, national origin, political opinions or affiliations. For more information on obtaining other UF/IFAS Extension publications, contact your county's UF/IFAS Extension office.

U.S. Department of Agriculture, UF/IFAS Extension Service, University of Florida, IFAS, Florida A & M University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Nick T. Place, dean for UF/IFAS Extension.