The vulnerability to drought-induced embolism-conduit diameter link: breaching the anatomy-physiology divide

Abstract

Summary The best explanations of the relationship between organismal form and function-those regarded by scientists as the most solid — always account for both comparative, across-species, patterns, as well as experimental results. This is true in all of biology, as it is for the study of xylem structure-function relations, where there is still a need for xylem physiology and functional comparative wood anatomy to mutually complement each other. To illustrate the magnitude and urgency of this need, we discuss Sherwin Carlquist’s postulate of a link between vulnerability to drought-induced embolism and conduit diameter, summarizing some of the major global patterns of xylem trait variation that are currently explained by postulating a vulnerability–diameter link. These include wider community mean and maximum vessel diameters in wetter vs drier vegetation types; that vessels can be >700 μm in diameter but plants virtually always produce much narrower ones; that dryland plants with wider vessels drop their leaves earlier; wide-to-narrow vessels across growth rings; and the wide vessels of lianas surrounded by narrow vessels. These patterns are global, and we are aware of no anatomical evidence contradicting a vulnerability–diameter link. Despite the pervasiveness of these patterns, many xylem biologists do not regard the patterns as providing guidance for research in functional xylem biology. Instead, proposing and testing hypotheses to account for all of the data — xylem physiology experiments and comparative anatomical patterns in all their complexity and with all of their contradictions — provides the best way forward for the field. This effort requires proposing and testing hypotheses that are consistent with both experimental as well as comparative data. Crucially, it also requires not rejecting the vulnerability–diameter link without providing an alternative explanation that better explains the patterns currently explained by appeal to the link.

Seasonal Cambial Activity and Formation of Secondary Phloem and Xylem in White Oaks (Quercus alba L.)

“…However, similarly to temperate species, tropical species also form the latewood long before the selective regime, contradicting this idea and suggesting a possible selective importance to narrow vessels in the tropical dry seasons as well. This scenario merits additional tests [48].…”

“…While narrow vessels have been accepted as safer against embolism caused by frost [40][41][42][43], the same is not true for embolism caused by drought [41,46], positing a problem. For decades, based on comparative wood anatomical studies, especially those championed by Carlquist [1,47,48], researchers have proposed that narrow vessels would be safer against drought embolism [49,50], such as the embolisms caused by frost. However, nowadays there is a heated debate among experimental wood anatomists, where one group's experiments seem to corroborate the hypothesis that narrow vessels are safer against drought embolism [49,50], while another's vehemently dispute that conclusion, demonstrating by their experiments that the decisive character promoting safety against drought embolism is the thickness of intervessel pit membranes [46].…”

Wood anatomy of Tabaroa, a monotypic papilionoid legume genus narrowly endemic to the Brazilian Caatinga seasonally dry tropical forests

“…Tabaroa caatingicola has a set of wood anatomy traits that distinguishes it from other Brongniartieae genera. The wood anatomy of T. caatingicola reveals a set of adaptations to the SDTFW biome of the Brazilian Caatinga domain, where the low precipitation with irregular rains, high temperatures, and high transpiration potential increases the likelihood of droughtinduced embolism formation (Hacke et al 2023;Olson et al 2023). These adaptations include semi-ring-porous wood with distinct growth ring boundaries, multiple narrow vessels, simple perforation plates, small and vestured pits.…”

A systems genetic analysis identifies putative mechanisms and candidate genes regulating vessel traits in poplar wood

“…Our understanding of the regulation of vessel traits in trees remains incomplete and there has been ongoing debate regarding whether vessel traits are at all directly genetically regulated or if they represent an indirect response to environmental conditions ( Olson et al, 2014 ; Olson et al, 2020 ). Emerging evidence gives strong support to the hypothesis that changes in wood development and resulting vessel traits are the result of coordinated regulation, however.…”