Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding

Resistance to water-stress induced cavitation is an important indicator of drought tolerance in woody species and is known to be intimately linked to the anatomy of the xylem. However, the actual mechanical properties of the pit membrane are not well known and the exact mode of air-seeding by which cavitation occurs is still uncertain. We examined the relationship between cavitation resistance and bordered pit structure and function in 40 coniferous species. Xylem pressure inducing 50% loss of hydraulic conductance (P50, a proxy for cavitation resistance) varied widely among species, from −2.9 to −11.3 MPa. The valve effect of the pit membrane, measured as a function of margo flexibility and torus overlap, explained more variation in cavitation-resistance than simple anatomical traits such as pit membrane, pit aperture or torus size. Highly cavitation resistant species exhibited both a high flexibility of the margo and a large overlap between the torus and the pit aperture, allowing the torus to tightly seal the pit aperture. Our results support the hypothesis of seal capillary-seeding as the most likely mode of air-seeding, and suggest that the adhesion of the torus to the pit border may be the main determinant of cavitation resistance in conifers

Balancing the risks of hydraulic failure and carbon starvation : a twig scale analysis in declining Scots pine

Understanding physiological processes involved in drought-induced mortality is important for predicting the future of forests and for modelling the carbon and water cycles. Recent research has highlighted the variable risks of carbon starvation and hydraulic failure in drought-exposed trees. However, little is known about the specific responses of leaves and supporting twigs, despite their critical role in balancing carbon acquisition and water loss. Comparing healthy (non-defoliated) and unhealthy (defoliated) Scots pine at the same site, we measured the physiological variables involved in regulating carbon and water resources. Defoliated trees showed different responses to summer drought compared with non-defoliated trees. Defoliated trees maintained gas exchange while non-defoliated trees reduced photosynthesis and transpiration during the drought period. At the branch scale, very few differences were observed in non-structural carbohydrate concentrations between health classes. However, defoliated trees tended to have lower water potentials and smaller hydraulic safety margins. While non-defoliated trees showed a typical response to drought for an isohydric species, the physiology appears to be driven in defoliated trees by the need to maintain carbon resources in twigs. These responses put defoliated trees at higher risk of branch hydraulic failure and help explain the interaction between carbon starvation and hydraulic failure in dying trees.Peer reviewe

Vulnerabilite a la cavitation de quelques especes forestieres feuillues et resineuses: aspects methodologiques, importance ecophysiologique

SIGLEAvailable from INIST (FR), Document Supply Service, under shelf-number : TD 81114 / INIST-CNRS - Institut de l'Information Scientifique et TechniqueFRFranc

Short-time xylem relaxation results in reliable quantification of embolism in grapevine petioles and sheds new light on their hydraulic strategy

In recent years, the validity of embolism quantification methods has been questioned, especially for long-vesseled plants. Some studies have suggested that cutting xylem while under tension, even under water, might generate artificial cavitation. Accordingly, a rehydration procedure prior to hydraulic measurements has been recommended to avoid this artefact. On the other hand, concerns have been raised that xylem refilling might occur when samples are rehydrated. Here, we explore the potential biases affecting embolism quantification for grapevine (Vitis vinifera L.) petioles harvested under tension or after xylem relaxation. We employ direct visualization of embolism through X-ray micro-computed tomography (microCT) to test for the occurrence of fast refilling (artifactually low per cent loss of conductivity (PLC) due to rehydration prior to sample harvest) as well as excision-induced embolism (artifactually high embolism due to air introduction during harvest). Additionally, we compared the response functions of both stomatal regulation and xylem embolism to xylem pressure (\u3a8x). Short-time (20\u2005min) xylem tension relaxation prior to the hydraulic measurement resulted in a lower degree of embolism than found in samples harvested under native tensions, and yielded xylem vulnerability curves similar to the ones obtained using direct microCT visualization. Much longer periods of hydration (overnight) were required before xylem refilling was observed to occur. In field-grown vines, over 85% of stomatal closure occurred at less negative \u3a8x than that required to induce 12% PLC. Our results demonstrate that relaxation of xylem tension prior to hydraulic measurement allows for the reliable quantification of native embolism in grapevine petioles. Furthermore, we find that stomatal regulation is sufficiently conservative to avoid transpiration-induced cavitation. These results suggest that grapevines have evolved a strategy of cavitation resistance, rather than one of cavitation tolerance (diurnal cycles of embolism and repair)

Is water stress induced embolism in grapevines a common phenomenon? Hints from MRI and microCT visualizations

Previous research suggested that grapevines are very vulnerable to water deficit induced embolism. Several authors found ~50% loss of conductivity (PLC) when stem water potentials (\u3a8S) where higher than -1 MPa. Because such \u3a8S are very common in vineyards, it was believed that drought induced cavitation is a frequent event. Moreover, since stomata regulation takes place at approximately similar \u3a8S, it was suggested that petiole cavitation could regulate stomatal closure. In the current research we performed in-vivo visualization of petioles and stems during dehydration using Magnetic Resonance Imaging (MRI) and synchrotron-based micro computed tomography (microCT). Additionally, an adjusted hydraulic protocol, that yielded comparable results to those of the visualization techniques, was utilized to compare PLC and stomatal closure in grapevines under water deficit. Our results show that grapevine petioles are more resistant to cavitation than previously presumed. 50% PLC or 50% embolized vessels were measured at \u3a8S of -1.3 to -1.5 MPa. Very few emboli (less than 10%) were noticed during the majority of stomatal down regulation (from 250 to less than 50 mmol m-2 s-1). Comparison of embolism in the stem and petiole showed that stems are even more resistant to embolism, reaching 50% embolized vessels at -2 MPa. These findings suggest that significant embolism does not commonly occur in grapevines. During water stress, stomatal down regulation will limit transpiration in order to avoid xylem cavitation. Only when that line of defense is breached, embolism in the petiole will hydraulically disconnect the leaves (i.e. evaporative surface) from the stem in order to maintain the stem\u2019s hydraulic integrity

Plasticity in vulnerability to cavitation of Pinus canariensis occurs only at the driest end of an aridity gradient

Water availability has been considered one of the crucial drivers of species distribution. However, the increasing of temperatures and more frequent water shortages could overcome the ability of long-lived species to cope with rapidly changing conditions. Growth and survival of natural populations adapted to a given site, transferred and tested in other environments as part of provenance trials, can be interpreted as a simulation of ambient changes at the original location. We compare the intraspecific variation and the relative contribution of plasticity to adaptation of key functional traits related to drought resistance: vulnerability to cavitation, efficiency of the xylem to conduct water and biomass allocation. We use six populations of Canary Island pine growing in three provenance trials (wet, dry, and xeric). We found that the variability for hydraulic traits was largely due to phenotypic plasticity, whereas, genetic variation was limited and almost restricted to hydraulic safety traits and survival. Trees responded to an increase in climate dryness by lowering growth, and increasing leaf-specific hydraulic conductivity by means of increasing the Huber value. Vulnerability to cavitation only showed a plastic response in the driest provenance trial located in the ecological limit of the species. This trait was more tightly correlated with annual precipitation, drought length, and temperature oscillation at the origin of the populations than hydraulic efficiency or the Huber value. Vulnerability to cavitation was directly related to survival in the dry and the xeric provenance trials, illustrating its importance in determining drought resistance. In a new climatic scenario where more frequent and intense droughts are predicted, the magnitude of extreme events together with the fact that plasticity of cavitation resistance is only shown in the very dry limit of the species could hamper the capacity to adapt and buffer against environmental changes of some populations growing in dry locations

Coordination of stem and leaf traits define different strategies to regulate water loss and tolerance ranges to aridity

Adaptation to drought involves complex interactions of traits that vary within and among species. To date, few data are available to quantify within-species variation in functional traits and they are rarely integrated into mechanistic models to improve predictions of species response to climate change. We quantified intraspecific variation in functional traits of two Hakea species growing along an aridity gradient in southeastern Australia. Measured traits were later used to parameterise the model SurEau to simulate a transplantation experiment to identify the limits of drought tolerance. Embolism resistance varied between species but not across populations. Instead, populations adjusted to drier conditions via contrasting sets of trait trade-offs that facilitated homeostasis of plant water status. The species from relatively mesic climate, Hakea dactyloides, relied on tight stomatal control whereas the species from xeric climate, Hakea leucoptera dramatically increased Huber value and leaf mass per area, while leaf area index (LAI) and epidermal conductance (gmin) decreased. With trait variability, SurEau predicts the plasticity of LAI and gmin buffers the impact of increasing aridity on population persistence. Knowledge of within-species variability in multiple drought tolerance traits will be crucial to accurately predict species distributional limits

Grapevine petioles are more sensitive to drought induced embolism than stems: Evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation

The \u2018hydraulic vulnerability segmentation\u2019 hypothesis predicts that expendable distal organs are more susceptible to water stress-induced embolism than the main stem of the plant. In the current work, we present the first in vivo visualization of this phenomenon. In two separate experiments, using magnetic resonance imaging or synchrotron-based microcomputed tomography, grapevines (Vitis vinifera) were dehydrated while simultaneously scanning the main stems and petioles for the occurrence of emboli at different xylem pressures (\u3a8x). Magnetic resonance imaging revealed that 50% of the conductive xylem area of the petioles was embolized at a \u3a8x of 121.54\u2009MPa, whereas the stems did not reach similar losses until 121.9\u2009MPa. Microcomputed tomography confirmed these findings, showing that approximately half the vessels in the petioles were embolized at a \u3a8x of 121.6\u2009MPa, whereas only few were embolized in the stems. Petioles were shown to be more resistant to water stress-induced embolism than previously measured with invasive hydraulic methods. The results provide the first direct evidence for the hydraulic vulnerability segmentation hypothesis and highlight its importance in grapevine responses to severe water stress. Additionally, these data suggest that air entry through the petiole into the stem is unlikely in grapevines during drought