Comparative anatomy vs mechanistic understanding: How to interpret the diameter-vulnerability link

Authors: LENS, FREDERIC - Naturalis Biodiversity Center; Gleason, Sean; BORTOLAMI, GIOVANNI - Naturalis Biodiversity Center; BRODERSEN, CRAIG - Yale University; DELZON, SYLVAIN - University Of Bordeaux; JANSEN, STEVEN - Ulm University

Submitted to: IAWA Journal (International Association of Wood Anatomists Journal)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/24/2023
Publication Date: 10/23/2023
Citation: Lens, F., Gleason, S.M., Bortolami, G., Brodersen, C., Delzon, S., Jansen, S. 2023. Comparative anatomy vs mechanistic understanding: How to interpret the diameter-vulnerability link. IAWA Journal(International Association of Wood Anatomists Journal). 44(3-4):368-380. https://doi.org/10.1163/22941932-bja10137.
DOI: https://doi.org/10.1163/22941932-bja10137

Interpretive Summary: Research on how plants cope with drought has long assumed that the internal water-conducting “pipes” inside vascular plants (vessels) should be more vulnerable to drought damage when they are wide, relative to when they are narrow. However, recent studies show that this assumption may not be accurate because the most likely causes of vessel damage occur at a very small scale inside the plant's structure. Therefore, a better understanding of the physical and chemical processes that occur at the nano-level is needed to accurately predict how water transport in plants is affected by drought. This new research opens up exciting opportunities to learn more about the complex interactions between plants and their environment.

Technical Abstract: Results from ecological wood anatomy in combination with experimental studies from the field of plant hydraulics have led to a pervasive and longstanding assumption that wider diameter vessels are more vulnerable to drought-induced embolism than narrower vessels. However, our current understanding of drought-induced embolism does not offer a mechanistic explanation for why increased vessel diameter should lead to greater vulnerability. Moreover, recent advances in the field of fluid transport suggest the most likely causes of embolism formation and spread operate at the nano-level (e.g., inside the 3D structure of intervessel pit membranes), not at the level of whole vessels. The mechanistic understanding of drought-induced embolism remains incomplete, however, but it also provides new opportunities for resolving key questions regarding its anatomical and physico-chemical drivers. We argue here that the observed correlation between embolism vulnerability and vessel diameter is most likely non-causal, whereas the most proximal determinants of embolism likely include intervessel pit membrane traits that have arisen independently from vessel diameter. As such, the observed correlation between vulnerability and vessel diameter in meta-analyses has limited value in informing our understanding of embolism formation, embolism spread between adjacent vessels, as well as the selective forces shaping the evolution of these traits. A meaningful evaluation of the diameter-vulnerability link will therefore require a better mechanistic understanding of the biophysical processes at the nano-scale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought.