Xylem embolism spreads by single-conduit events in three dry forest angiosperm stems

Johnson, Kate M.

doi:10.46678/pb.20.1374643

Cited by 10 publications

(19 citation statements)

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“…This technique has the advantage of being noninvasive, allowing cavitation to be monitored in real time during dehydration. Although the technique does not directly measure changes in hydraulic conductance, it has been shown to accurately visualize xylem cavitation events (Johnson et al, 2020) and if used correctly produces results that are highly comparable with flow methods (Gauthey et al, 2020). Briefly, transmitted light images of intact leaves were captured plants dehydrated under laboratory conditions (22°C and 40-50% relative humidity).…”

Section: Leaf Xylem Vulnerability To Cavitationmentioning

confidence: 99%

Linking xylem network failure with leaf tissue death

et al. 2021

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Summary Global warming is expected to dramatically accelerate forest mortality as temperature and drought intensity increase. Predicting the magnitude of this impact urgently requires an understanding of the process connecting atmospheric drying to plant tissue damage. Recent episodes of forest mortality worldwide have been widely attributed to dry conditions causing acute damage to plant vascular systems. Under this scenario vascular embolisms produced by water stress are thought to cause plant death, yet this hypothetical trajectory has never been empirically demonstrated. Here we provide foundational evidence connecting failure in the vascular network of leaves with tissue damage caused during water stress. We observe a catastrophic sequence initiated by water column breakage under tension in leaf veins which severs local leaf tissue water supply, immediately causing acute cellular dehydration and irreversible damage. By highlighting the primacy of vascular network failure in the death of leaves exposed to drought or evaporative stress our results provide a strong mechanistic foundation upon which models of plant damage in response to dehydration can be confidently structured.

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Section: Leaf Xylem Vulnerability To Cavitationmentioning

confidence: 99%

Linking xylem network failure with leaf tissue death

et al. 2021

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“…Methods that are capable of visualizing individual embolism events support the idea that individual embolism events will occur over a wide range of water potentials in many species in both stem and leaf xylem (Jacobsen et al 2019;Venturas et al 2016;Johnson et al 2020;Knipfer et al 2015). In stems the first embolism events are often observed near the primary xylem (Choat et al 2015a), or in some cases the largest volume vessels (Jacobsen et al 2019;Johnson et al 2020;Knipfer et al 2015), suggesting these conduits embolise first. In leaves, the first embolism events are almost always observed in the midrib and proceed, as leaf water potential declines, through the increasingly higher orders of veins (Skelton et al 2017;Brodribb et al 2016a;Scoffoni et al 2017b).…”

Section: Introductionmentioning

confidence: 82%

“…In angiosperms, pore constrictions in multi-layered pit membranes and/or a relatively high degree of isolation within the hydraulic conduit network provides added protection from the spreading of pre-existing embolism into water-filled conduits during drought (Johnson et al 2020;Schenk et al 2008;Avila et al 2021). The narrow size of pore constrictions (< 50 nm) and the highly variable pore size dimensions do not allow mass flow of gas from an embolised to a water-filled conduit under negative pressure (Yang et al 2020;Kaack et al 2019;Kaack et al 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Other factors might also provide an explanation for the greater absence of embolism occurrence in angiosperm xylem after rehydration and on a second cycle of dehydration until reaching the Ψ at which the branch was rehydrated, including the increased separation of conduits imbedded in a matrix of non-conductive xylem tissue, such as fibres and parenchyma that might offer a physical barrier for rapid air propagation through the xylem (Johnson et al 2020;Avila et al 2021), particularly compared to the tracheid based xylem of conifers, which is largely homogeneous and comprised of closely packed tracheids. The close proximity of tracheids with tracheid tips slightly bent and overlapping multiple neighbouring tracheids may facilitate a more rapid spread of embolism on a second dehydration cycle in conifers (Torres-Ruiz et al 2016;Choat et al 2015b), while the 3D reconstruction of vessel networks deserves more attention for angiosperms (Wason et al 2021).…”

Section: Discussionmentioning

confidence: 99%

“…This range of water potential is typically quantified by the slope of vulnerability curves, with a narrow range and a steep slope characterising vulnerable species, and a wider range and flatter slope more embolism resistant species (Kaack et al 2021). Methods that are capable of visualizing individual embolism events support the idea that individual embolism events will occur over a wide range of water potentials in many species in both stem and leaf xylem (Jacobsen et al 2019;Venturas et al 2016;Johnson et al 2020;Knipfer et al 2015). In stems the first embolism events are often observed near the primary xylem (Choat et al 2015a), or in some cases the largest volume vessels (Jacobsen et al 2019;Johnson et al 2020;Knipfer et al 2015), suggesting these conduits embolise first.…”

Section: Introductionmentioning

confidence: 99%

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Xylem embolism spread is largely prevented by interconduit pit membranes until the majority of conduits are gas-filled

Avila¹,

Guan²,

Kane³

et al. 2021

Preprint

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Xylem embolism resistance varies across species influencing drought tolerance, yet little is known about the determinants of the embolism resistance of an individual conduit. Here we conducted an experiment using the optical vulnerability method to test whether individual conduits have a specific water potential threshold for embolism formation and whether pre-existing embolism in neighbouring conduits alters this threshold. Observations were made on a diverse sample of angiosperm and conifer species through a cycle of dehydration, rehydration and subsequent dehydration to death. Upon rehydration after the formation of embolism, no refilling was observed. When little pre-existing embolism was present, xylem conduits had a conserved, individual, embolism resistance threshold that varied across the population of conduits. The consequence of a variable conduit-specific embolism threshold is that a small degree of pre-existing embolism in the xylem results in an apparently more resistant xylem in a subsequent dehydration, particularly in angiosperms with vessels. While our results suggest that pit membranes separating xylem conduits are critical for maintaining a conserved individual embolism threshold for given conduit when little pre-exisiting embolism is present, as the percentage of embolized conduits increases, gas movement, local pressure differences, and connectivity between conduits increasingly contribute to embolism spread.

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Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks

Skelton

Anderegg

Díaz

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks (Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below −2.7 MPa in all 19 species, and −6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere’s most ecologically and economically important plants.

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Xylem embolism spreads by single-conduit events in three dry forest angiosperm stems

Cited by 10 publications

References 0 publications

Linking xylem network failure with leaf tissue death

Linking xylem network failure with leaf tissue death

Xylem embolism spread is largely prevented by interconduit pit membranes until the majority of conduits are gas-filled

Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks

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