How Leaf Trait Trade-Offs Mediated Proteomic Reconfiguration in Drought-Primed Olive Plants in Response to Terminal Drought?

Drought priming has been recognized as a strategy to enhance drought stress resilience in various plants; however its mechanistic basis remains scarce, particularly for woody species like olive. Here, olive plants (Olea europaea L.) were firstly exposed to drought for three weeks followed by water recovery time (two months) and then subjected to subsequent severe drought (one month). Results showed that non-primed plants (NPP) exhibited a dramatic decrease of photosynthesis, water status and growth due to a severe reduction in the leaf area, leading to inhibition of light energy capture and carbon fixation, together with an alteration of key proteins implicated in photosynthesis and nitrogen metabolism. Conversely, physiological performances of drought primed plants (PP) were improved under terminal drought. This state was achieved through a coordinated morpho-physiological regulation, which involved a controlled stomata conductance coupled to a moderate leaf area reduction towards optimizing water conservation and carbon fixation. Regulation in total leaf lipid content, fatty acid unsaturation and the enhanced lignin content seem crucial for membrane function, water retention and tissue stability. Ultimately, such adjustments were reflected harmonically in the corresponding proteomic profile. Indeed, key proteins involved in CO2 assimilation, those governing PSII efficiency, electron transport and nitrogen metabolism proved the pivotal role of priming in protecting the metabolism of PP. Overall, priming induced complex modulation of leaf traits coupled with fine molecular regulation, enabling olive to better tolerate stress and to convert it into “beneficial stress imprint” improving their water use efficiency.