Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms

SummaryEmbolism spreading in angiosperm xylem occurs via mesoporous pit membranes between vessels. Here, we investigate how the size of pore constrictions in pit membranes is related to pit membrane thickness and embolism resistance.In three models, pit membranes are modelled as multiple layers to investigate how pit membrane thickness and the number of intervessel pits per vessel determine pore constriction sizes, the probability of encountering large pores, and air-seeding. These estimations were complemented by measurements of pit membrane thickness, embolism resistance, and number of intervessel pits per vessel (n = 31, 31, and 20 species, respectively).Constriction sizes in pores decreased with increasing pit membrane thickness, which agreed with the measured relationship between pit membrane thickness and embolism resistance. The number of pits per vessel affected constriction size and embolism resistance much less than pit membrane thickness. A strong relationship between estimated air-seeding pressures and measured embolism resistance was observed.Pore constrictions provide a mechanistic explanation why pit membrane thickness determines embolism resistance, and suggest that hydraulic safety can be uncoupled from hydraulic efficiency. Although embolism spreading remains puzzling and encompasses more than pore constriction sizes, angiosperms are unlikely to have leaky pit membranes, which enables tensile transport of water.

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The Pneumatron estimates xylem embolism resistance in angiosperms based on gas diffusion kinetics: a mini-review

Acta Horticulturae ◽

10.17660/actahortic.2020.1300.25 ◽

2020 ◽

pp. 193-200

Author(s):

S. Jansen ◽

X. Guan ◽

L. Kaack ◽

C. Trabi ◽

M.T. Miranda ◽

...

Keyword(s):

Gas Diffusion ◽

Diffusion Kinetics ◽

Xylem Embolism ◽

Embolism Resistance

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Embolism resistance in petioles and leaflets of palms

Annals of Botany ◽

10.1093/aob/mcz104 ◽

2019 ◽

Vol 124 (7) ◽

pp. 1173-1183 ◽

Cited By ~ 3

Author(s):

Thaise Emilio ◽

Laurent J Lamarque ◽

José M Torres-Ruiz ◽

Andrew King ◽

Guillaume Charrier ◽

...

Keyword(s):

Hydraulic Conductivity ◽

Xylem Embolism ◽

Phylogenetic Relatedness ◽

X Ray ◽

Xylem Pressure ◽

Palm Species ◽

Embolism Resistance ◽

Increasing Temperature

Abstract Background and aims Hydraulic studies are currently biased towards conifers and dicotyledonous angiosperms; responses of arborescent monocots to increasing temperature and drought remain poorly known. This study aims to assess xylem resistance to drought-induced embolism in palms. Methods We quantified embolism resistance via P50 (xylem pressure inducing 50 % embolism or loss of hydraulic conductivity) in petioles and leaflets of six palm species differing in habitat and phylogenetic relatedness using three techniques: in vivo X-ray-based microcomputed tomography, the in situ flow centrifuge technique and the optical vulnerability method. Key results Our results show that P50 of petioles varies greatly in the palm family, from −2.2 ± 0.4 MPa in Dypsis baronii to −5.8 ± 0.3 MPa in Rhapis excelsa (mean ± s.e.). No difference or weak differences were found between petioles and leaf blades within species. Surprisingly, where differences occurred, leaflets were less vulnerable to embolism than petioles. Embolism resistance was not correlated with conduit size (r = 0.37, P = 0.11). Conclusions This study represents the first estimate of drought-induced xylem embolism in palms across biomes and provides the first step towards understanding hydraulic adaptations in long-lived arborescent monocots. It showed an almost 3-fold range of embolism resistance between palm species, as large as that reported in all angiosperms. We found little evidence for hydraulic segmentation between leaflets and petioles in palms, suggesting that when it happens, hydraulic segregation may lack a clear relationship with organ cost or replaceability.

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Linking drought‐induced xylem embolism resistance to wood anatomical traits in Neotropical trees

New Phytologist ◽

10.1111/nph.16942 ◽

2020 ◽

Vol 229 (3) ◽

pp. 1453-1466

Author(s):

Sébastien Levionnois ◽

Steven Jansen ◽

Ruth Tchana Wandji ◽

Jacques Beauchêne ◽

Camille Ziegler ◽

...

Keyword(s):

Xylem Embolism ◽

Neotropical Trees ◽

Embolism Resistance

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

10.22541/au.162864525.54313554/v1 ◽

2021 ◽

Author(s):

Rodrigo Avila ◽

Xinyi Guan ◽

Cade Kane ◽

Amanda Cardoso ◽

Timothy Batz ◽

...

Keyword(s):

Drought Tolerance ◽

Water Potential ◽

Small Degree ◽

Conifer Species ◽

Local Pressure ◽

Xylem Embolism ◽

Embolism Resistance ◽

Potential Threshold ◽

Xylem Conduits

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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Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique

Journal of Experimental Botany ◽

10.1093/jxb/erz474 ◽

2019 ◽

Vol 71 (3) ◽

pp. 1151-1159 ◽

Cited By ~ 9

Author(s):

Danielle Creek ◽

Laurent J Lamarque ◽

José M Torres-Ruiz ◽

Camille Parise ◽

Regis Burlett ◽

...

Keyword(s):

Water Stress ◽

Stomatal Closure ◽

Safety Margin ◽

Carbon Assimilation ◽

Xylem Embolism ◽

Growth And Survival ◽

Direct Observations ◽

Optical Visualization ◽

Embolism Resistance ◽

The One

Abstract Drought represents a major abiotic constraint to plant growth and survival. On the one hand, plants keep stomata open for efficient carbon assimilation while, on the other hand, they close them to prevent permanent hydraulic impairment from xylem embolism. The order of occurrence of these two processes (stomatal closure and the onset of leaf embolism) during plant dehydration has remained controversial, largely due to methodological limitations. However, the newly developed optical visualization method now allows concurrent monitoring of stomatal behaviour and leaf embolism formation in intact plants. We used this new approach directly by dehydrating intact saplings of three contrasting tree species and indirectly by conducting a literature survey across a greater range of plant taxa. Our results indicate that increasing water stress generates the onset of leaf embolism consistently after stomatal closure, and that the lag time between these processes (i.e. the safety margin) rises with increasing embolism resistance. This suggests that during water stress, embolism-mediated declines in leaf hydraulic conductivity are unlikely to act as a signal for stomatal down-regulation. Instead, these species converge towards a strategy of closing stomata early to prevent water loss and delay catastrophic xylem dysfunction.

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Prediction of temperate broadleaf tree species mortality in arid limestone habitats with stomatal safety margins

Tree Physiology ◽

10.1093/treephys/tpz045 ◽

2019 ◽

Vol 39 (8) ◽

pp. 1428-1437 ◽

Cited By ~ 2

Author(s):

Zhicheng Chen ◽

Shan Li ◽

Junwei Luan ◽

Yongtao Zhang ◽

Shidan Zhu ◽

...

Keyword(s):

Tree Species ◽

Tree Mortality ◽

Vascular System ◽

Stomatal Closure ◽

Survival Rates ◽

Safety Margin ◽

Xylem Embolism ◽

Safety Margins ◽

Broadleaf Tree ◽

Embolism Resistance

Abstract A growing body of evidence highlights the occurrence of increased widespread tree mortality during climate change-associated severe droughts; however, in situ long-term drought experiments with multispecies communities for the prediction of tree mortality and exploration of related mechanisms are rather limited in natural environments. We conducted a 7-year afforestation trial with 20 drought-resistant broadleaf tree species in an arid limestone habitat in northern China, where the species displayed a broad range of survival rates. The stomatal and xylem hydraulic traits of all the species were measured. We found that species’ stomatal closure points were strongly related to their xylem embolism resistance and xylem minimum water potential but not to their survival rates. Hydraulic failure of the vascular system appeared to be the main cause of tree mortality, and the stomatal safety margin was a better predictor of tree mortality than the traditionally considered xylem embolism resistance and hydraulic safety margin. We recommend the stomatal safety margin as the indicator for predicting drought-induced tree mortality and for selecting tree species in future forest restorations in arid regions.

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