Physiological and transcriptomic analyses reveal that VPD modifies CO2 fertilization effect on tomato plants via abscisic acid and jasmonic acid signaling pathways

Abstract

Atmospheric CO2 concentration is elevated globally, which has “CO2 fertilization effects” and potentially improves plant photosynthesis, yield, and productivity. Despite the beneficial effect of CO2 fertilization being modulated by vapor pressure deficit (VPD), the underlying mechanism is highly uncertain. In the present study, the potential roles of hormones in determining CO2 fertilization effects under contrasting high and low VPD conditions were investigated by integrated physiological and transcriptomic analyses. Beneficial CO2 fertilization effects were offset under high VPD conditions and were constrained by plant water stress and photosynthetic CO2 utilization. High VPD induced a large passive water driving force, which disrupted the water balance and consequently caused plant water deficit. Leaf water potential, turgor pressure, and hydraulic conductance declined under high VPD stress. The physiological evidence combined with transcriptomic analyses demonstrated that abscisic acid (ABA) and jasmonic acid (JA) potentially acted as drought-signaling molecules in response to high VPD stress. Increased foliar ABA and JA content triggered stomatal closure to prevent excessive water loss under high VPD stress, which simultaneously increased the diffusion resistance for CO2 uptake from atmosphere to leaf intercellular space. High VPD also significantly increased mesophyll resistance for CO2 transport from stomatal cavity to fixation site inside chloroplast. The chloroplast “sink” CO2 availability was constrained by stomatal and mesophyll resistance under high VPD stress, despite the atmospheric “source” CO2 concentration being elevated. Thus, ABA- and JA-mediated drought-resistant mechanisms potentially modified the beneficial effect of CO2 fertilization on photosynthesis, plant growth, and yield productivity. This study provides valuable information for improving the utilization efficiency of CO2 fertilization and a better understanding of the physiological processes.