Abstract
Mi-1.2 is a single dominant gene in tomato that confers race-specific resistance against certain phloem-feeding herbivores including aphids, whiteflies, psyllids, and root-knot nematodes. Few prior studies have considered the potential non-target effects of race-specific resistance genes (R genes), and this paper evaluates the compatibility of Mi-mediated resistance in tomato with a beneficial zoophytophagous predator, Orius insidiosus (Say). In addition to preying on aphids and other pests, this piercing-sucking insect also feeds from the xylem, epidermis, and/or mesophyll, and oviposits within plant tissues. Comparison of O. insidiosus confined to isogenic tomato plants with and without Mi-1.2 revealed that immatures of O. insidiosus had lower survival on resistant plants even when the immatures were provisioned with prey that did not feed on the host plant. Molecular gut content analysis confirmed that adults and immatures of O. insidiosus feed on both resistant (Mi-1.2+) and susceptible (Mi-1.2-) genotypes, and bioassays suggest that resistance does not affect oviposition rates, plant sampling, or prey acceptance by O. insidiosus adults. These results demonstrate a direct negative impact of R-gene-mediated host plant resistance on a non-target beneficial species, and reveal that Mi-mediated resistance can impact organisms that do not feed on phloem sap. Through laser capture microdissection and RT-PCR, Mi-1.2 transcripts were detected in the epidermis and mesophyll as well as the phloem of tomato plants, consistent with our observations that Mi-mediated resistance is active outside the phloem. These results suggest that the mode of action and potential ecological impacts of Mi-mediated resistance are broader than previously assumed.
Highlights
Insect-resistant crop varieties and biological con- many of the resistance mechanisms that protect plants from trol agents are both important components of integrated pest herbivorous insects may deter beneficial predatory management, they are not always fully compatible, because insects
To determine whether exposure to resistant plants has any direct effects on O. insidiosus, adults were allowed to oviposit on intact tomato plants, and rates of oviposition, emergence, and offspring survival were compared on three genotypes: a tomato cultivar that lacks Mi-1.2
Offspring were provisioned with moth eggs from artificial diet-reared laboratory cultures to ensure that the quality of prey provided to the O. insidiosus was unaffected by the host plants; the high O. insidiosus mortality observed on genotypes that carry Mi-1.2 can be attributed to direct interactions between the plant and the predators
Summary
Insect-resistant crop varieties and biological con- many of the resistance mechanisms that protect plants from trol agents are both important components of integrated pest herbivorous insects may deter beneficial predatory management, they are not always fully compatible, because insects. To assess the costs, benefits, and ecological impacts of host plant resistance, it is critical to examine the effects of resistance on biological control agents. Most studies on the effects of host plant resistance on biological control agents have focused on fairly broad-spectrum defences that persist over time and are expressed throughout the plant, such as trichomes or insecticidal transgenes (Ode, 2006; Gatehouse et al, 2011). Fewer studies have examined the potential non-target impacts of monogenic resistance genes (R genes) in plants. These genes typically confer resistance against one or a small number of pest species, and may not be effective against all biotypes within the target species. It is important to test the target range of R gene-mediated resistance empirically
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