Elevated CO2 and plant-insect interactions: Connecting gene expression to ecological responses

The compensatory feeding hypothesis posits that by increasing the carbon:nitrogen ratio (C:N), growth under elevated CO₂ will increase herbivory by folivorous insects. Exposure of field-grown soybean to elevated levels of CO₂ anticipated by 2050 increased the concentration of soluble sugars and starch in leaves and also increased foliar herbivory by Japanese beetles, western corn rootworm, and soybean aphids. Consuming foliage grown under elevated CO₂ increased longevity and fitness of Japanese beetles, but elevated leaf carbohydrates or C:N could not explain these changes. Analysis of the soybean transcriptome with microarrays revealed that under field conditions key genes coding for the production of jasmonic acid (JA), an important plant defense hormone, were down-regulated under elevated CO₂. Lower constitutive levels and a dampened induction of JA following beetle herbivory reduced expression of the gene coding for cysteine protease inhibitor (CystPI), a defense employed by soybean against insects. Consistent with the reduction in soybean CystPI, Japanese beetles consuming foliage grown under elevated CO₂ had greater gut protease activity; more efficient digestion of leaves grown under elevated CO₂ may have contributed to increased fitness of Japanese beetles. By ignoring variation in plant defenses, the compensatory feeding hypothesis may incorrectly invoke C:N ratios as the explanation for enhanced feeding in the context of elevated CO₂. At least for the soybean agro-ecosystem, ever increasing levels of CO₂ in the atmosphere may increase herbivory by dampening hormonal signaling and chemical defense.