关键词: 叶脉, 气孔, 解剖结构, 耦合适应, 叶形分化, 胡杨异形叶

Abstract: Aims Leaves, exhibiting the highest ecological plasticity, are the most sensitive to environmental change. It also acts as the hydraulic bottleneck and safety valve against hydraulic dysfunctions. Populus euphratica Oliv. is well-adapted to extreme arid environments and possess heteromorphic leaves distributing differentially along tree vertical heights. Exploring the pattern variations of hydraulic and anatomical traits of heteromorphic leaves and their interaction, and underpinning mechanisms of morphological divergence along groundwater depth(GWD) and vertical heights is better understanding their adaptation strategies to adverse environment, so as to provide a scientific basis for protection and restoration of desert P. euphratica forest under global change. Methods Through community investigation along GWD, we measured the hydraulic, structural and morphological traits in three different leaf shapes of adult P. euphratica trees along canopy vertical height. The differences between hydraulic traits (e.g., Hydraulic conductance, vein, stomata), anatomical structures and morphological traits of heteromorphic leaves and their interrelationships were examined. Important findings (1) Under different GWD conditions, significant differences were observed in the morphological, hydraulic and anatomical traits of leaves with the same morphology, while under the same GWD, three heteromorphic leaves exhibited notable variations in these traits across different canopy heights. For the same leaf shape, the minor vein density, loopiness of veins, free-end density, conduit density, leaf thickness, palisade-to-spongy mesophyll ratio, epidermal and cuticular thickness increased with rising GWD, while these traits increased along vertical canopy height under the same GWD. Deeper GWD and higher canopy positions were associated with enhanced vein development and more xeromorphic anatomical structures in heteromorphic leaves. (2) Compared to the heteromorphic leaves in the lower-middle canopy, the serrated broad-oval leaves in the upper canopy are wider and thicker, with more developed palisade tissue and complex venation networks. These structural adaptations have evolved to cope with strong light, high temperature and increased transpiration demands, resulting in a more efficient hydraulic system and strongly defensive architecture, enhancing the water transport efficiency and water retention capacity, thereby improving embolism resistance and drought tolerance. (3) The leaf length-width ratio (LI) and dissection index (DI) were significantly correlated with most hydraulic and anatomical traits. Hydraulic traits contributed more to leaf morphological variation than anatomical features, with interval between veins, closed loop area, vein density, proportion of minor veins, as well as palisade-spongy ratio, epidermal and cuticular thickness playing predominant roles in shaping leaf morphology. (4) Most leaf morphological traits showed a highly significant correlation with hydraulic path length and leaf attachment height. Hydraulic path length mediates leaf morphological variation (LI, DI) by influencing hydraulic and anatomical structures, indicating that hydraulic constraints along vertical gradient are a key factor driving leaf morphological differentiation in P. euphratica. (5) The coupling between hydraulic traits and anatomical structures contributes to improve hydraulic functionality and enhanced stress resilience in P. euphratica. Leaf morphological differentiation represents an ecological strategy evolved by the species to adapt contrasting hydraulic environments throughout its life cycle.

Key words: leaf vein, stomata, anatomical structure, coupling adaptation, morphological differentiation, heteromorphic leaves of Populus euphratica Oliv.