Aerial and underground organs display specific metabolic strategies to cope with water stress under rising atmospheric CO in Fagus sylvatica L.

Beech is known to be a moderately drought-sensitive tree species, and future increases in atmospheric concentrations of CO ([CO ]) could influence its ecological interactions, also with changes at the metabolic level. The metabolome of leaves and roots of drought-stressed beech seedlings grown under two different [CO ] (400 (aCO ) and 800 (eCO ) ppm) was analyzed together with gas exchange parameters and water status. Water stress estimated from predawn leaf water potential (Ψ ) was similar under both [CO ], although eCO had a positive impact on net photosynthesis and intrinsic water use efficiency. The aerial and underground organs showed different metabolomes. Leaves mainly stored C metabolites, while those of N and P accumulated differentially in roots. Drought triggered the proline and N-rich amino acids biosynthesis in roots through the activation of arginine and proline pathways. Besides the TCA cycle, polyols and soluble sugar biosynthesis were activated in roots, with no clear pattern seen in the leaves, prioritizing the root functioning as metabolites sink. eCO slightly altered this metabolic acclimation to drought, reflecting mitigation of its effect. The leaves showed only minor changes, investing C surplus in secondary metabolites and malic acid. The TCA cycle metabolites and osmotically active substances increased in roots, but many other metabolites decreased as if the water stress was dampened. Above- and belowground plant metabolomes were differentially affected by two drivers of climate change, water scarcity and high [CO ], showing different chemical responsiveness that could modulate the tree adaptation to future climatic scenarios.