Data from: Repeated origin of three-dimensional leaf venation releases constraints on the evolution of succulence in plants

Succulent water storage is a prominent feature among plants adapted to arid zones, but we know little about how succulence evolves and how it is integrated into organs already tasked with multiple functions. Increased volume in succulent leaves, for example, may result in longer transport distances between veins and the cells that they supply, which in turn could negatively impact photosynthesis [1, 2, 3 and 4]. We quantified water storage [5] in a group of 83 closely related species to examine the evolutionary dynamics of succulence and leaf venation. In most leaves, vein density decreased with increasing succulence, resulting in significant increases in the path length of water from veins to evaporative surfaces. The most succulent leaves, however, had a distinct three-dimensional (3D) venation pattern, which evolved 11–12 times within this small lineage, likely via multiple developmental pathways. 3D venation “resets” internal leaf distances, maintaining moderate vein density in extremely succulent tissues and suggesting that the evolution of extreme succulence is constrained by the need to maintain an efficient leaf hydraulic system. The repeated evolution of 3D venation decouples leaf water storage from hydraulic path length, facilitating the evolutionary exploration of novel phenotypic space.

储水肉质特性是适应干旱生境植物的显著特征，但我们对肉质化（succulence）的演化路径，以及其如何与已承担多重功能的器官实现整合的机制仍所知有限。例如，肉质叶片的体积增大，可能会延长叶脉与其供养细胞间的运输距离，进而可能对光合作用产生负面影响[1, 2, 3, 4]。我们针对83个近缘物种组成的类群开展了储水能力量化研究[5]，以此探究肉质化与叶片脉序（venation）的演化动力学。在多数叶片中，叶脉密度随肉质化程度提升而降低，导致水分从叶脉至蒸发表面的运输路径长度显著增加。然而，肉质化程度最高的叶片具有独特的三维（3D）脉序模式，该模式在该小型演化支（lineage）中独立演化了11至12次，其背后可能涉及多种发育途径。三维脉序能够"重置"叶片内部的距离限制，在极度肉质化的组织中维持适中的叶脉密度，这表明极端肉质化的演化受到维持高效叶片水力系统（hydraulic system）的需求约束。三维脉序的反复演化将叶片储水能力与水力路径长度解耦，为探索全新的表型空间（phenotypic space）提供了演化上的便利。