Herbivore perception decreases photosynthetic carbon assimilation and reduces stomatal conductance by engaging 12-oxo-phytodienoic acid, mitogen-activated protein kinase 4 and cytokinin perception

Herbivory-induced changes in photosynthesis have been documented in many plant species; however, the complexity of photosynthetic regulation and analysis has thwarted progress in understanding the mechanism involved, particularly those elicited by herbivore-specific elicitors. Here, we analysed the early photosynthetic gas exchange responses in Nicotiana attenuata plants after wounding and elicitation with Manduca sexta oral secretions and the pathways regulating these responses. Elicitation with M. sexta oral secretions rapidly decreased photosynthetic carbon assimilation (AC) in treated and systemic (untreated, vascularly connected) leaves, which were associated with changes in stomatal conductance, rather than with changes in Rubisco activity and 1-5 ribulose-1,5-bisphosphate turnover. Phytohormone profiling and gas exchange analysis of oral secretion-elicited transgenic plants altered in phytohormone regulation, biosynthesis and perception, combined with micrografting techniques, revealed that the local photosynthetic responses were mediated by 12-oxo-phytodienoic acid, while the systemic responses involved interactions among jasmonates, cytokinins and abscisic acid signalling mediated by mitogen-activated protein kinase 4. The analysis also revealed a role for cytokinins interacting with mitogen-activated protein kinase 4 in CO2-mediated stomatal regulation. Hence, oral secretions, while eliciting jasmonic acid-mediated defence responses, also elicit 12-oxo-phytodienoic acid-mediated changes in stomatal conductance and AC, an observation illustrating the complexity and economy of the signalling that regulates defence and carbon assimilation pathways in response to herbivore attack.