A novel mechanism for resistance to Colorado potato beetle (Leptinotarsa decemlineata) in wild Solanum species

The Colorado potato beetle (Leptinotarsa decemlineata Say) is the most destructive insect pest of the potato (Solanum tuberosum L.) worldwide and has shown remarkable adaptability to insecticides. In wild Solanum species, the best known host-plant resistance mechanisms are a high level of foliar glycoalkaloids and the presence of specialized, glandular trichomes. Through a preliminary field-test screen, three Solanum species, Solanum trifidum, S. raphanifolium, and S. circaeifolium, were identified with low foliar glycoalkaloid levels and no glandular trichomes, but still exhibiting substantial resistance to L. decemlineata. These three species along with two species, S. berthaultii and S. chacoense, representing the two known mechanisms of resistance, were examined in bioassays for larval leaf consumption, effect on larval growth, and percent larval mortality. The best S. trifidum accessions had approximately ten-fold less foliar consumption per larva than controls and induced 54% reduction in larval weight compared to controls during a 24 h feeding period. Forty-eight h mortality rates were 100% for second and third instars feeding on S. trifidum compared to 22% for the S. tuberosum controls. Despite very low foliar glycoalkaloid levels and the absence of glandular trichomes, S. trifidum accessions exhibited both an effective antinutritive and deterrent mechanism for resistance to L. decemlineata. In a further effort to identify the resistance mechanism(s), proteinase inhibitor activity in these resistant species was studied. Plant proteinase inhibitors function as a defense mechanism against feeding insects by disrupting gut proteolytic digestion. Potato multicystatin (PMC) is a member of the cystatin superfamily of cysteine proteinase inhibitors and is effective in retarding insect growth by inhibiting the cysteine proteinases commonly found in the guts of numerous beetle species. Two of the species, S. chacoense and S. berthaultii, have known resistance mechanisms, whereas, S. trifidum exhibits a novel host-plant resistance mechanism against the Colorado potato beetle. PMC induction occurred in all three resistant species in response to methyl jasmonate treatment and wounding by beetle feeding. Two of the resistant species showed very high levels of PMC activity as measured by papain inhibition in response to beetle feeding. It is likely that PMC activity in the resistant species serves as an antinutrutive mechanism of defense but is only one component in the plant's overall defense system.