University of FloridaSolutions for Your Life

Download PDF
Publication #HS1259

The Good, the Bad, and the Ugly: What the Future Could Hold for Bs2 Tomatoes1

S. F. Hutton, J. W. Scott, J. B. Jones, R. E. Stall, G. E. Vallad, B. J. Staskawicz, and D. M. Horvath 2

Over the past several years there has been considerable discussion within the Florida tomato industry about Bs2 tomatoes. Previous and ongoing trials conducted by University of Florida researchers have consistently and repeatedly demonstrated the benefits of these cultivars for bacterial spot disease management, while growers and industry members who have visited these trials likewise recognize the potential for Bs2 tomatoes to make Florida tomato production a much more sustainable operation. But what does the future really hold for this technology? What benefits might be realized by the adoption of Bs2 tomato varieties, and what challenges stand in the way of their commercial production?

What Are Bs2 Tomatoes?

Bs2 tomatoes are transgenic tomatoes that have been engineered to contain the Bs2 gene from pepper. As such, they are considered a genetically modified (GM) food, or a genetically modified organism (GMO). (For more information about GMOs see Schneider, Schneider, and Richardson 2002). Bs2 transgenic tomatoes were developed by the Two Blades Foundation, a charitable scientific organization, which holds an exclusive license to the Bs2 gene, in collaboration with scientists at the University of California and the University of Florida.

Bacterial spot is a major disease of both pepper and tomato, especially in Florida and other warm, humid production regions of the world. Plant resistance is desired because chemical control is costly and sometimes ineffective when conditions are favorable for development of the disease. In pepper, conventional (non-GMO) breeding efforts have been very successful due to the discovery and use of several individual resistance genes. Seven of these resistance genes have been reported (Potnis et al. 2012; Stall, Jones, and Minsavage 2009), four of which have been exploited in commercial varieties (Bs1, Bs2, Bs3, and bs5). The majority of these genes behave in a manner consistent with the gene-for-gene hypothesis devised by Henry Flor (1955). By this model, a resistance gene in the plant must recognize a corresponding gene, commonly referred to as an avirulence gene, in the bacterium in order for the plant to be resistant; thus both genes are necessary for resistance to bacterial spot. In most cases where single resistance genes are deployed, crops remain disease-free for a period of time (usually a few years), until a mutation occurs in the pathogen’s avirulence gene, rendering the corresponding resistance gene ineffective. This was the case with pepper varieties containing Bs2 alone, which became available in 1984 (Cook 1984) and were widely grown in the 1990s. But after only several years, bacteria containing mutations in the Bs2 avirulence gene became prevalent in the field (Pernezny and Collins 1999), and when deployed alone, Bs2 resistance was no longer effective against such strains. Fortunately, not all pathogen strains carry a mutant Bs2 avirulence gene (Wichmann 2005), and pepper breeders have enjoyed some success against bacterial spot by pyramiding Bs2 with other resistance genes (for example, Bs2 combined with Bs3). This strategy also helps prolong the “life” of the resistance genes, since the pathogen can only survive/spread if mutations occur in all avirulence genes at the same time.

In contrast to pepper, tomato breeders have been unsuccessful in developing bacterial spot resistant varieties by conventional approaches. Although the UF/IFAS tomato breeding program has maintained an active breeding project for resistance since the early 1980s, no resistant varieties have been developed. There are several reasons for this, including limited sources of resistance, resistance that is conferred by multiple genes rather than a single gene (which makes the breeding process much more complicated), mutations in pathogen avirulence genes resulting in ineffective resistance genes, and introduction of exotic pathogen strains which overcome the resistance (Hutton et al. 2010). In short, tremendous efforts on the breeding front have been unable to combine horticultural acceptability with high levels of resistance in tomato.

The Bs2 gene from pepper was cloned in the late 1990s when the gene conferring resistance was identified (Tai et al. 1999).The researchers also determined that transgenic tomatoes containing the pepper Bs2 gene were resistant to bacterial spot. Because of the difficulty in developing resistant tomato varieties by conventional means, many have considered Bs2 tomatoes an important tool to manage this devastating disease.

The Good

There are several reasons why Bs2 tomatoes are an attractive strategy for management of bacterial spot:

  • The Bs2 gene occurs naturally in plants. What is more, it occurs naturally in a major food crop, pepper. The protein product of the Bs2 gene is safe for consumption, attested to by more than two decades of the public’s consumption of bell peppers containing Bs2.

  • The Bs2 gene provides excellent disease control in tomatoes (Figure 1). This was demonstrated in a multi-year experiment where Bs2 tomatoes maintained extremely low levels of disease compared to susceptible controls, while inbred lines with conventionally-bred resistance had intermediate levels of infection (Horvath et al. 2012).

  • Figure 1. 

    Bacterial spot resistance in tomato conferred by the pepper Bs2 gene. On the left are symptomless Bs2 transgenic plants of the hybrid, Fla. 8314; on the right are severely infected non-transgenic plants of the cultivar VF36. The picture was taken from a trial conducted in Florida in spring 2012, for which all plants in the trial were inoculated with the bacterial spot pathogen.


    [Click thumbnail to enlarge.]

  • Bs2 is effective against all field strains of the tomato bacterial spot pathogen. This was determined by surveying bacteria samples from the production regions of Florida and parts of Georgia; all strains contained a recognizable Bs2 avirulence gene, meaning that Bs2 would provide effective resistance throughout the southeast production region (Horvath et al. 2012). Additionally, many of the mutations which have occurred in the Bs2 avirulence gene and which provide the pathogen a means to escape detection by the resistance gene also result in a loss of fitness of the bacterium (Kearny and Staskawicz 1990), meaning that the mutant strains are often weaker and less likely to survive and/or cause severe infections.

  • Higher yields are obtained with Bs2 tomatoes. In repeated trials, Bs2 inbreds and hybrids maintain a 1.5-fold or greater yield increase over the non-transgenic versions of these inbreds and hybrids; when conditions were favorable for disease, these increases were often 2-fold or greater (Horvath et al., 2012, 2014).

  • Bs2 tomatoes are a green technology. Because these tomatoes have a significant yield advantage over traditional varieties, increased production can be realized without increasing fertilizer, pesticide, plastic, or other inputs. Thus the carbon footprint per unit of production can be reduced. In addition, because Bs2 tomatoes provide good control for bacterial spot, copper and other chemical sprays for management of this disease can be reduced or eliminated, which can further reduce environmental impact.

  • The Bs2 gene is a simple, highly effective tool for tomato breeders to utilize. As described above, most of the conventionally bred resistance is controlled by multiple genes, meaning that breeders have to sift through many more plants to identify those that are most resistant. Furthermore, unlike the resistance provided by the Bs2 gene, current conventionally bred resistance genes only provide tolerance or partial resistance; thus breeders spend a great deal more time and effort trying to distinguish between “shades of gray,” vs. presence or absence of disease.

The Bad

Although years of repeated trials have demonstrated the ability of the Bs2 gene to effectively eliminate bacterial spot in tomatoes, the success of this gene in tomatoes hinges on its ability to recognize the pathogen’s Bs2 avirulence gene. So if mutations occur in the Bs2 avirulence gene (which they will) that prevent recognition, Bs2 could be rendered ineffective at controlling bacterial spot of tomato. As was discussed earlier, this is what occurred in non-transgenic Bs2 pepper varieties in only a matter of years. In fact, such mutations already have been observed on a limited scale in Bs2 tomato trials (Horvath et al. 2014).

In order to prolong the “life” of Bs2 resistant tomatoes, care will need to be taken to limit the emergence and spread of resistance-breaking strains. Several strategies are available, any number of which might be employed.

  • Deployment of Bs2 exclusively in varieties that contain conventionally bred tolerance or partial resistance to bacterial spot. This is a good strategy because a pathogen must simultaneously overcome multiple mechanisms of resistance. But this is easier said than done because of the challenges of conventional breeding for tolerance or partial resistance conferred by multiple genes, as already discussed.

  • Employment of cultural practices to minimize the emergence and spread of mutant strains of the pathogen. Further research is needed to identify helpful strategies that are not already practiced. Ultimately, those cultural practices that are based on good sanitation all the way from seed production to the growers’ fields will go a long way to minimize bacterial spot outbreaks and the introduction of resistance-breaking strains.

  • Deployment of Bs2 in combination with other novel resistance genes. As scientists expand their understanding of plant disease resistance, there will no doubt be additional resistance genes discovered—whether in relatives of tomato, in other Solanaceous species, or in entirely different plant families—and some of these genes may provide useful levels and alternative mechanisms of resistance. As long as these genes do not rely on recognition of the same avirulence gene in the pathogen, the pyramiding of Bs2 with one or more of these likely would prove extremely long-lasting. This strategy of pyramiding resistance genes to promote their durability is not novel; examples include combining multiple conventionally bred resistance genes to Striga in sorghum (Ejeta 2007), as well as pyramiding multiple transgenic insect resistance genes in cotton (Li et al. 2014).

The Ugly

There currently are no Bs2 tomatoes being produced for sale or consumption, and this will not change until two hurdles are passed. The first is the de-regulation process. It takes years for a transgenic crop to be de-regulated, and the process is costly. The Two Blades Foundation has invested significant resources toward the development and testing of this GMO. However, additional funds are needed in order to complete the de-regulation process, and many potential investors are wary due to concerns about public acceptance—which is the second hurdle.

Even though this gene has the potential to increase yields while decreasing pesticide applications, and even though it is naturally present in peppers, which are very closely related to tomatoes, the Bs2 resistance gene does not naturally occur in tomatoes. Since peppers and tomatoes cannot be intercrossed, the only way to utilize this gene in tomatoes is through the use of transgenic technology. Ultimately, because growers will only produce what they can sell, the future of Bs2 tomatoes relies on whether or not the public will accept and buy their product.

Going Forward

If deployed carefully, Bs2 tomatoes have the potential to significantly advance the sustainability of tomato production in bacterial spot-prone environments by increasing yields while reducing pesticide inputs. The Bs2 protein product is known to be safe based on decades of its consumption in pepper. But before Bs2 tomatoes can be grown, the de-regulation process must be completed; and before Bs2 tomatoes will be grown, producers must be satisfied that they can sell their product. Thus public controversy over GMO technology has everything to do with the future of Bs2 tomatoes.

Although there is considerable opposition to and great skepticism over GM technology, it is evident that much of this is based on the public’s perception of the science. A recent Intelligence Squared U.S. debate illustrated this: after hearing concerns over GMOs addressed by both GMO-skeptics and by supporters of GMO technology, an audience changed from 32% supportive of GM technology before the debate, to 60% afterward (Fraley et al. 2014). The opinion shift after that debate suggests that increasing acceptance of Bs2 tomatoes (and other GMOs) will depend on transparency and open discussion between scientists and the general public to show these crops’ benefits to consumers, growers, and the environment..

Literature Cited

Cook, A. A. 1984. “Florida XVR 3-25 Bell Pepper.” HortScience 19:735.

Ejeta, G. 2007. “Breeding for Resistance in Sorghum: Exploitation of an Intricate Host-Parasite Biology.” Crop Sci. 47:S216–S227.

Flor, H. H. 1955. “Host-Parasite Interactions in Flax Rust—Its Genetics and Other Implications.” Phytopathology 45:680–685.

Fraley, R., A. V. Eenennaam, C. Benbrook, and M. Mellon. “Genetically Modified Food.” Intelligence Squared U.S. Debate. Kaufman Center, New York. 3 Dec. 2014. Debate. http://intelligencesquaredus.org/debates/past-debates/item/1161-genetically-modify-food.

Horvath, D. M., S. F. Hutton, G. E. Vallad, J. B. Jones, R. E. Stall, D. Dahlbeck, B. J. Staskawicz, D. Tricoli, A. V. Deynze, M. H. Pauly, and J. W. Scott. 2014. “The Pepper Bs2 Gene Confers Effective Field Resistance to Bacterial Leaf Spot and Yield Enhancement in Florida Tomatoes.” Acta Hort. (in press).

Horvath, D. M., R. E. Stall, J. B. Jones, M. H. Pauly, G. E. Vallad, D. Dahlbeck, B. J. Staskawicz, and J. W. Scott. 2012. “Transgenic Resistance Confers Effective Field Level Control of Bacterial Spot Disease in Tomato.” PLoS ONE 7(8):e42036.

Hutton, S. F., J. W. Scott, W. Yang, S. C. Sim, D. M. Francis, and J. B. Jones. 2010. ”Identification of QTL Associated with Resistance to Bacterial Spot Race T4 in Tomato.” Theoretical and Applied Genetics 121(7):1275–1287.

Kearney, B. and B. J. Staskawicz. 1990. “Widespread Distribution and Fitness Contribution of Xanthomonas campestris pv. Vesicatoria Avirulence Gene avrBs2.” Nature 346:385–386.

Li, L., Y. Zhu, S. Jin, and X. Zhang. 2014. “Pyramiding Bt Genes for Increasing Resistance of Cotton to Two Major Lepidopteran Pests: Spodoptera litura and Heliothis armigera.” Acta Physiol. Plant 36:2717–2727.

Pernezny, K. and J. Collins. 1999. “A Serious Outbreak of Race 6 of Xanthomonas campestris pv. Vesicatoria on Pepper in Southern Florida.” Plant Dis. 83:79.

Potnis, N., G. Minsavage, J. K. Smith, J. C. Hurlbert, D. Norman, R. Rodrigues, R. E. Stall, and J .B. Jones. 2012. “Avirulence Proteins AvrBs7 from Xanthomonas gardneri and AvrBs1.1 from Xanthomonas euvesicatoria Contribute to a Novel Gene-for-Gene Interaction in Pepper.” Mol. Plant Microbe Interact. 25:307–320.

Schneider, K. R., R. G. Schneider, and S. Richardson. 2002. “Genetically Modified Food.” FSHN02-2. Gainesville, FL: University Florida Institute of Food and Agricultural Sciences. http://edis.ifas.ufl.edu/fs084.

Stall, R. E., J. B. Jones, and G. V. Minsavage. 2009. “Durability of Resistance in Tomato and Pepper to Xanthomonads Causing Bacterial Spot.” Annu. Rev. Phytopathol. 47:265–284.

Tai, T. H., D. Dahlbeck, E. T. Clark, P. Gajiwala, R. Pasion, M. C. Whalen, R. E. Stall, and B. J. Staskawicz. 1999. “Expression of the Bs2 Pepper Gene Confers Resistance to Bacterial Spot Disease in Tomato.” Proc. Natl. Acad. Sci. USA 96:14153–14158.

Wichmann, G., D. Ritchie, C. S. Kousik, and J. Bergelson. 2005. “Reduced Genetic Variation Occurs among Genes of the Highly Clonal Plant Pathogen Xanthomonas axonopodis pv. Vesicatoria, Including the Effector Gene avrBs2.” Appl. Envir. Microb. 71:2418–2432.

Footnotes

1.

This document is HS1259, one of a series of the Horticultural Sciences Department, UF/IFAS Extension. Original publication date April 2015. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

S. F. Hutton, assistant professor, Horticultural Sciences Department, UF/IFAS Gulf Coast Research and Education Center, Wimauma, FL; J.W. Scott, professor, Horticultural Sciences Department, Gulf Coast Research and Education Center, UF/IFAS Extension, Wimauma, FL; G. E. Vallad, associate professor, Horticultural Sciences Department, Gulf Coast Research and Education Center, UF/IFAS Extension, Wimauma, FL; J.B. Jones, professor, Plant Pathology Department, UF/IFAS Extension, Gainesville, FL; R. E. Stall, emeritus professor, Plant Pathology Department, UF/IFAS Extension, Gainesville, FL; B. J. Staskawicz, professor, Department of Plant and Microbial Biology, University of California, Berkeley, CA; and D. M. Horvath, Two Blades Foundation, Evanston, IL


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.