Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores

• Published in: Oecologia Vol. 174; no. 3; pp. 883 - 892
• Main Authors: Kersch-Becker, Mônica F, Thaler, Jennifer S
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer-Verlag 01-03-2014; Springer; Springer Berlin Heidelberg; Springer Nature B.V
• Subjects: Animal and plant ecology; Animal, plant and microbial ecology; Animals; Aphididae; Aphids - physiology; Beetles; Biological and medical sciences; Biomedical and Life Sciences; Caterpillars; Coleoptera - physiology; Community structure; correlation; Development and progression; Disease transmission; Ecology; Fecundity; Fundamental and applied biological sciences. Psychology; General aspects; Genetic vectors; Health aspects; Herbivores; Herbivory; Host plants; Host-Pathogen Interactions; Hydrology/Water Resources; Infection; Infections; insect communities; Insect vectors; Insect Vectors - physiology; Insect Vectors - virology; Insecta - physiology; Insects; Larva - physiology; Leptinotarsa decemlineata; Life Sciences; Lycopersicon esculentum; Lycopersicon esculentum - physiology; Lycopersicon esculentum - virology; Macrosiphum euphorbiae; Mastication; Microbiology; Moths - physiology; Pathogens; Plant Diseases; Plant Growth Regulators - metabolism; Plant resistance; Plant Sciences; PLANT-MICROBE-ANIMAL INTERACTIONS; Plant-microbe-animal interactions - Original research; Plants; Potato virus Y; Potatoes; Potyvirus - physiology; Replicative cycle, interference, host-virus relations, pathogenicity, miscellaneous strains; Tomatoes; Trichoplusia ni; Virology; Viruses; Salicylic acid; Aphids; Vector–virus interactions; Plant resistance; Induced responses; Aphidoidea; Vector-virus interactions; Herbivorous; Insecta; Interaction; Virus; Sensitivity resistance; Homoptera; Arthropoda; Aphididae; Invertebrata; Vector
• ISSN: 0029-8549; 1432-1939
• DOI: 10.1007/s00442-013-2812-7

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVYᴺᵀᴺ, PVYᴺᴼ and PVYᴼ) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVYᴺᵀᴺ induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVYᴺᵀᴺ infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect–plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.