High metabolic sensitivity to hot drought in two declining pine species with constrained physiology

Abstract

Decline syndromes preceding tree mortality under increased abiotic stress often include reductions in transpiring leaf area and tree growth. However, the mechanisms regulating the metabolism and physiology of declining trees before they cross irreversible thresholds in their performance under hotter drought are not fully understood. We characterized physiological and metabolic adjustments in Pinus sylvestris and Pinus pinaster forests currently experiencing decline and high mortality rates. These two species have different ecological requirements and drought tolerances, yet they express similar long-term decline syndromes under increased hot drought stress. The physiological and metabolic adjustments of trees were coherent with sensitive functional responses to high abiotic stress characteristic of tree decline. Although trees operated above their hydraulic safety margins, the hydraulic function was more impaired in declining trees, particularly of P. sylvestris. Declining trees maintained negative but reversible leaf turgor under summer hot drought for longer periods than healthy trees. Leaf-level gas exchange was more downregulated in declining than in healthy trees only under peak summer drought stress. The leaf metabolic expression under peak summer hot drought between healthy and declining trees differed and discriminated between health status better than the leaf-level physiological spectrum. Metabolic adjustments affected several interrelated metabolic pathways where the accumulation of different primary and secondary compounds in declining trees was either enhanced (e.g. D-pinitol, L-proline) or inhibited (e.g. sucrose, raffinose) compared to those in healthy trees. Estimated levels of carbohydrates show no carbon depletion in trees of any health status. Trees with long-term constrained physiological performance expressed an idiosyncratic but complex metabolic response under hot drought that characterized the decline syndrome prior to mortality in the studied pine species. Read the free Plain Language Summary for this article on the Journal blog.