Herbivore induction of jasmonate-dependent defenses reduces photosynthesis in Nicotiana attenuata

Background/Question/Methods

Herbivory often forces the plant under attack to reallocate resources from growth to the production of secondary metabolites for defense. In Nicotiana species the induction of plant defenses reorganizes plant metabolism to produce toxic feeding deterrents and results in reduced plant growth and fitness. However, the mechanisms by which growth decreases are not well understood. In this study we used plants with modified jasmonic acid (JA)-based defenses to characterize the physiological responses of N. attenuata plants under herbivory. If the induction of chemical defenses corresponds to a decrease in photosynthesis, representing a reallocation of resources, we predict that plants with disable defense ability should suffer a smaller reduction in photosynthesis following herbivory than wild type (WT) plants. This hypothesis was tested by comparing photosynthesis following herbivory by the specialist herbivore, Manduca sexta, in WT plants and plants where defenses have been silenced (antisense mutants of lipoxygenase3; LOX, putrescine methyl transferase; PMT). We measured leaf photosynthesis using an open-system infrared gas analyzer coupled with a chlorophyll fluorescence imaging system and verified concentrations of leaf secondary metabolites using liquid chromatography and mass spectrometry.

Results/Conclusions

All plants suffered reduced photosynthesis with immediate defoliation (24h and 3d continuous damage). The operating quantum efficiency of photosystem II (ФPSII) was reduced in visibly undamaged tissues adjacent to damaged tissue and this area of reduction was twice as great in WT plants as in LOX plants. This suggests that the induction of defenses alters the capacity (and efficiency) for electron transport in tissues adjacent to damage. When plants were allowed to recover from herbivory, photosynthesis immediately recovered to undamaged levels in LOX plants; however, plants with defense signaling intact (WT, PMT) suffered reduced photosynthetic capacity for up to five days after the herbivore attack. These results suggest there is a direct functional tradeoff between mounting an effective chemical defense in N. attenuata and maintaining high rates of photosynthesis. This reduction in photosynthesis may explain how the induction of JA-related defenses in Nicotiana species ultimately reduces growth and fitness.