Impacts of a virus resistant transgene on the establishment and spread of powdery mildew in wild squash

Background/Question/Methods

Gene exchange between crops and their wild relatives is common and difficult to contain.  Unlike most traits of cultivated species, there are concerns that transgenes conferring resistance to herbivores or pathogens could enhance the fitness and weediness of wild species and/or have indirect impacts on non-target species such as pollinators, herbivores, predators, soil fauna, and other plants in the community.  Gene flow between cultivated squash and its wild counterpart (Cucurbita pepo ssp. texana) may result in the introduction of a virus resistant transgene (VRT) that confers resistance to three common viruses in wild populations.  We have extensively studied the interactions among C. pepo, its primary herbivores (cucumber beetles and aphids), and the pathogens they transmit (Erwinia tracheiphila, the causative agent of bacterial wilt, and three mosaic viruses) and found that the fitness of the transgene during escape is influenced by the full ecological community.  Indirect costs associated with increased exposure to herbivory by cucumber beetles and the bacterial wilt disease they transmit can mitigate the fitness benefits of the VRT.  Recent evidence suggests that viral infection negatively impacts the establishment and spread of a third pathogen in our system, powdery mildew, further mitigating the fitness benefits of the VRT. 

Results/Conclusions

We consistently find that a higher proportion of transgenic plants remain healthy during the growing season as they are susceptible to only one of the pathogens present in our system. As a consequence, transgenic plans are both more likely to reproduce and yield a greater number of fruits compared to susceptible wild squash.  These results would suggest that transgenic plants have a strong selective advantage.  However, we find that the fruit production of transgenic plants is only marginally greater than that of non-transgenic plants. In part, this can be explained by increased exposure of transgenic plants to Erwinia. Additionally, we find that powdery mildew symptoms are reduced on plants that have been previously infected with virus.  Data show that healthy plants get proportionally more powdery mildew than virus infected plants.  As a consequence, during widespread viral epidemics, transgenic plants get proportionally more powdery mildew than non-transgenic plants further reducing the benefits of the VRT.  Additionally, powdery mildew symptoms are significantly more severe on non-viral infected plants.  These results suggest that viral infection induces systemic acquired resistance, thereby reducing plant susceptibility to powdery mildew infection.  Because transgenic plants remain healthy during viral outbreaks, they are disproportionately affected by powdery mildew.