The role of soluble sugars and starch in plant-herbivore interactions : signaling and ecological consequences

Insect attack leads to a strong reconfiguration of plant metabolome, which influences the performance of the attacker. While the causes and consequences of induced changes in plant secondary metabolites are well studied, less is known about primary metabolites. To contribute to filling this gap of knowledge, I studied the role of sugars and starch in the interaction between Nicotiana attenuata and Manduca sexta. I found that M. sexta attack decreases soluble carbohydrates in N. attenuata leaves and roots. I did not observe this effect in jasmonate-deficient plants, suggesting that jasmonates are a plant signal that reprograms carbohydrate metabolism. Based on the above, I evaluated the ecological consequences of the observed jasmonate-dependent carbohydrate depletion in the context of plant resistance and tolerance by asking: Does the impact of M. sexta attack on leaf carbohydrates affect plant nutritional value and plant resistance? And does it reduce the capacity of roots to supply energy for regrowth and herbivore tolerance? Finally, I evaluated the degree of phylogenetic conservatism of the impact of M. sexta attack on both root carbohydrate reconfiguration and tolerance in the Solanaceae. My results suggest that i) lower sugar concentrations in the leaves lead to an increased M. sexta growth, suggesting that leaf carbohydrate depletion constrains rather than enhances plant resistance against herbivores; ii) the depletion of root carbohydrates significantly constrains the plant’s regrowth capacity and fitness, indicating that root carbohydrate depletion constrains tolerance to herbivory; and iii) changes in soluble root carbohydrate pools are strongly correlated with regrowth capacity across several solanaceous plant species and iv) that both traits do not show a phylogenetic signal, indicating that root carbohydrates are important determinants of tolerance to aboveground herbivory and that these two traits are subject of rapid evolution in the Solanaceae.