Out on a Limb: Testing the Hydraulic Vulnerability Segmentation Hypothesis in Trees Across Multiple Ecosystems

Plant Cell Environ. 2024 Nov 19. doi: 10.1111/pce.15249. Online ahead of print.

Abstract

Plant hydraulic theory states that leaf and stem vulnerability to embolism is coordinated within individual plants. The hydraulic vulnerability segmentation hypothesis (HVSH) predicts higher vulnerability in leaves to protect the stem from hydraulic failure, preserving stem xylem, which is generally more metabolically expensive and slower to regenerate than leaf tissues. However, studies designed to test HVSH have reported wide ranges in vulnerability segmentation (VS), and patterns with the environment have been elusive. In this study, we tested HVSH in phylogenetically constrained tree species from contrasting ecosystems across the Australian landscape. In 12 species, we found no support for HVSH. While leaf vulnerability was strongly governed by climate, VS was universally absent or negative. Consistently, the onset of leaf embolism occurred after the loss of leaf turgor and seasonally low leaf water potentials, illustrating the rarity of embolism in leaves. Within the leaf, embolism primarily occurring first and last in the leaf midvein, suggesting redundancy in leaf architecture to preserve function. Overall, this multi-ecosystem study provides a more complete picture of drought resistance mechanisms: (1) leaf safety was greatest in trees from drier ecosystems and (2) hydraulic thresholds were mostly conserved across organs indicating environmentally driven drought resistance in both leaves and stems.

Keywords: drought; leaf vulnerability; plant hydraulics; vulnerability segmentation; xylem embolism.