Water relations of a tropical vine-like bamboo (Rhipidocladum racemiflorum): root pressures, vulnerability to cavitation and seasonal changes in embolism

The occurrence of root pressure, the vulnerability of xylemvessels to drought-induced cavitation, and the seasonal changesin hydraulic conductivity due to embolism were studied in theculms of Rhipidocladum racemiflorum (Steud.) McClure, a tropicalvine-like bamboo from central Panama. Positive hydrostatic potentialsup to 120 kPa occurred only during the wet season when the transpirationrate of the plant was low, i.e. at night or during rain events.Although the xylem vessels were large and efficient for conductingwater, they were highly resistant to cavitation. Xylem waterpotentials lower than –4.5 MPa were required to induce50% loss of hydraulic conductivity in culms. The minimum waterpotential reached –3.75 MPa at the end of the 1993 dryseason, so loss of hydraulic conductivity due to embolism remained<10%. The species is adapted to drier habitats both by wayof a low vulnerability to xylem cavitation and by root pressuresin the wet season that could refill vessels that became embolizedduring a severe dry season. Key words: Rhipidocladum racemiflorum, root pressure, cavitation, embolism, water relations     

Water stress induced cavitation and embolism in some woody plants

A comparison was made of the relative vulnerability of xylem conduits to cavitation and embolism in three species [ Thuja occidentalis L., Tsuga canadensis (L.) Carr. and Acer saccharum Marsh.]. Waterlogged samples of wood were air dehydrated while measuring relative water loss, loss of hydraulic conductance, cumulative acoustic emissions (= cavitations) and xylem water potential. Most cavitation events and loss of hydraulic conductance occurred while water potential declined from – 1 to –6 MPa. There were differences in vulnerability between species. Other people have hypothesized that large xylem conduits (e.g. vessels) should be more vulnerable to cavitations than small conduits (e.g. tracheids). Our findings are contrary to this hypothesis. Under water stress, the vessel bearing wood retained water better than tracheid bearing wood. However, within a species large conduits were more prone to cavitation than small conduits.     

The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L.

We assessed the effects of irradiance received during growth on the vulnerability of Fagus sylvatica L. xylem vessels to water-stress-induced embolism. The measurements were conducted on (1) potted saplings acclimated for 2 years under 100% and 12% incident global radiation and (2) branches collected from sun-exposed and shaded sides of adult trees. Both experiments yielded similar results. Light-acclimated shoots were less vulnerable to embolism. Xylem water potential levels producing 50% loss of hydraulic conductivity were lower in sun-exposed branches and seedlings than in shade-grown ones (–3·0 versus –2·3 MPa on average). The differences in vulnerability were not correlated with differences in xylem hydraulic conductivity nor vessel diameter. Resistance to cavitation was correlated with transpiration rates, midday xylem and leaf water potentials in adult trees. We concluded that vulnerability to cavitation in Fagus sylvatica may acclimate to contrasting ambient light conditions.     

Shoot hydraulic characteristics, plant water status and stomatal response in olive trees under different soil water conditions

Aims

To evaluate the impact of the amount and distribution of soil water on xylem anatomy and xylem hydraulics of current-year shoots, plant water status and stomatal conductance of mature ‘Manzanilla’ olive trees.

Methods

Measurements of water potential, stomatal conductance, hydraulic conductivity, vulnerability to embolism, vessel diameter distribution and vessel density were made in trees under full irrigation with non-limiting soil water conditions, localized irrigation, and rain-fed conditions.

Results

All trees showed lower stomatal conductance values in the afternoon than in the morning. The irrigated trees showed water potential values around ?1.4 and ?1.6 MPa whereas the rain-fed trees reached lower values. All trees showed similar specific hydraulic conductivity (K _s) and loss of conductivity values during the morning. In the afternoon, K _s of rain-fed trees tended to be lower than of irrigated trees. No differences in vulnerability to embolism, vessel-diameter distribution and vessel density were observed between treatments.

Conclusions

A tight control of stomatal conductance was observed in olive which allowed irrigated trees to avoid critical water potential values and keep them in a safe range to avoid embolism. The applied water treatments did not influence the xylem anatomy and vulnerability to embolism of current-year shoots of mature olive trees.     

Vulnerability of xylem to embolism in a mangrove vs an inland species of Rhizophoraceae

Vulnerability of xylem conduits to cavitation and embolism was compared in two species of Rhizophoraceae, the mangrove Rhizophora mangle L. and the tropical moist-forest Cassipourea elliptica (Sw.) Poir. Cavitation (water column breakage preceeding embolism) was monitored by ultrasonic detection; embolism was quantified by its reduction of xylem hydraulic conductivity. Acoustic data were not predictive of loss in hydraulic conductivity, probably because signals from cavitating vessels were swamped by more numerous ones from cavitating fibers. Rhizophora mangle was the less vulnerable to embolism of the two species, losing 80% of its hydraulic conductivity between – 6.0 and – 7.0 MPa. Cassipourea elliptica lost conductivity in linear proportion to decreasing xylem pressure from – 0.5 to – 7.0 MPa. Species vulnerability correlated closely with physiological demands of habitat; the mangrove Rhizophora mangle had field xylem pressures between – 2.5 and – 4.0 MPa. whereas the minimum for Cassipourea elliptica was – 1.6 MPa. Differences in vulnerability between species could be accounted for by differences in the measured air permeability of intervessel pit membranes. According to this explanation, embolism occurs when air enters a water-filled vessel from a neighboring air-filled one via pores in shared pit membranes.     

Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance

Water transport through the xylem is essential for replacing water loss during transpiration, thus preventing desiccation and permitting photosynthesis. The occurrence of cavitation and embolism due to drought impairs transport to the transpiring leaves. Most research in this discipline has been conducted on woody plants. Less attention has been given to cavitation of crops and its physiological significance for understanding crop water relations. In this paper, hydraulic conductance and vulnerability of xylem to cavitation were studied in corn hybrids with different drought resistances. The results indicated that stems of drought-resistant ‘Pioneer 3902’ not only had a higher conductivity on both a stem area and leaf area basis but also had a greater resistance to cavitation. The estimated xylem pressure at 63.2% loss of conductivity (Weibull fitting parameter b) and at 50% loss of conductivity (P₅₀) in ‘Pioneer 3902’ were about 0.2 MPa lower than in ‘Pride 5’. Higher conductivity in ‘Pioneer 3902’ was mainly attributed to more vascular bundles per stem area rather than greater vessel diameter. The central bundles and peripheral vascular bundles showed the same degree of cavitation although the vessels of central bundles were generally larger than in peripheral bundles.     

Water loss regulation to soil drought associated with xylem vulnerability to cavitation in temperate ring-porous and diffuse-porous tree seedlings

Key message

Sustainable stomatal opening despite xylem cavitation occurs in ring-porous species and stomatal closure prior to cavitation in diffuse-porous species during soil drought.

Abstract

To elucidate the relationship between water loss regulation and vulnerability to cavitation associated with xylem structure, stomatal conductance (g _s), defoliation, vulnerability curves, and vessel features were measured on seedlings of ring-porous Zelkova serrata and Melia azedarach, and diffuse-porous Betula platyphylla var. japonica, Cerasus jamasakura and Carpinus tschonoskii. Under prolonged drought conditions, the percentage loss of hydraulic conductivity (PLC) increased and g _s decreased gradually with decreasing predawn (Ψ_pd) or xylem water potential (Ψ_xylem) in Z. serrata. During the gentle increase of PLC in M. azedarach, g _s increased in the early stages of dehydration while leaves were partly shed. A sharp reduction in g _s was observed before the onset of an increase in the PLC for drying plants of the three diffuse-porous species, suggesting cavitation avoidance by stomatal regulation. In the ring-porous species, xylem-specific hydraulic conductivity (K _s) was higher, whereas the vessel multiple fractions, the ratio of the number of grouped vessels to total vessels, was lower than that in the diffuse-porous species, suggesting that many were distributed as solitary vessels. This may explain the gradual increase in the PLC with decreasing Ψ_xylem because isolated vessels provide less opportunity for air seeding. Different water loss regulation to soil drought was identified among the species, with potential mechanisms being sustainable gas exchange at the expense of xylem dysfunction or partial leaf shedding, and the avoidance of xylem cavitation by strict stomatal regulation. These were linked to vulnerability to cavitation that appears to be governed by xylem structural properties.     

Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L.

Differences in the seasonal variation in stem water potential between the two shrub species Sorbus aucuparia and Sambucus nigra were related with their vulnerability to xylem cavitation. It was also demonstrated indirectly that the two species differ in the extent to which they reverse cavitation. Seasonal variation in stem water potential was investigated during three growing seasons with in situ stem psychrometers. Sorbus experienced wide water potential variations and reached a minimum of -4.2 MPa during drought. Under the same microclimatic conditions, Sambucus experienced consistent stem water potentials with a minimum of -1.7 MPa. The relationship between percentage loss in hydraulic conductivity (PLC) and water potential (hydraulic vulnerability curve) of the two species differed in shape: a flat curve with nearly total loss of conductivity at -6 MPa was found for SORBUS: Sambucus showed a steep vulnerability curve with 90% loss conductivity at -2.2 MPa. Thus, Sambucus is extremely vulnerable to cavitation, but Sorbus is an almost invulnerable species. This different cavitation resistance adjusted the ranges of field stem water potential that the species experienced. Finally, seasonal courses of naturally occurring (native) embolism were compared with calculated PLC courses. This comparison indicates that Sorbus did not refill embolized xylem vessels whereas Sambucus reversed embolism. It was concluded that species which are highly vulnerable to cavitation and drought-induced embolism need refilling of embolized vessels as well as isohydric water potential patterns as two strategies of survival.     

Poplar vulnerability to xylem cavitation acclimates to drier soil conditions

Xylem vulnerability to cavitation differs between tree species according to their drought resistance, more xerophilous species being more resistant to xylem cavitation. Variability in xylem vulnerability to cavitation is also found within species, especially between in situ populations. The origin of this variability has not been clearly identified. Here we analyzed the response of xylem hydraulic traits of Populus tremula×Populus alba trees to three different soil water regimes. Stem xylem vulnerability was scored as the xylem water potential causing 12, 50 and 88% loss of conductivity (P₁₂, P₅₀ and P₈₈). Vulnerability to cavitation was found to acclimate to growing conditions under different levels of soil water content, with P₅₀ values of ?1.82, ?2.03 and ?2.45 MPa in well‐watered, moderately water‐stressed and severely water‐stressed poplars, respectively. The value of P₁₂, the xylem tension at which cavitation begins, was correlated with the lowest value of midday leaf water potential (ψm) experienced by each plant, the difference between the two parameters being approximately 0.5 MPa, consistent with the absence of any difference in embolism level between the different water treatments. These results support the hypothesis that vulnerability to cavitation is a critical trait for resistance to drought. The decrease in vulnerability to cavitation under growing conditions of soil drought was correlated with decreased vessel diameter, increased vessel wall thickness and a stronger bordered pit field (t/b)². The links between these parameters are discussed.     

Interactive effects of water stress and xylem-limited bacterial infection on the water relations of a host vine

Xylella fastidiosa, a xylem-limited bacterial pathogen that causes bacterial leaf scorch in its hosts, has a diverse and extensive host range among plant species worldwide. Previous work has shown that water stress enhances leaf scorch symptom severity and progression along the stem in Parthenocissus quinquefolia infected by X. fastidiosa. The objective here was to investigate the mechanisms underlying the interaction of water stress and infection by X. fastidiosa. Using the eastern deciduous forest vine, P. quinquefolia, infection and water availability were manipulated while measuring leaf water potentials (psi(L)), stomatal conductance (g(s)), whole shoot hydraulic conductance (K(h)), per cent xylem embolism, and xylem vessel dimensions. No significant differences in any of the physiological measurements were found between control and infected plants prior to drought. Drought treatment significantly reduced psi(L) and g(s) at all leaf positions throughout the day in late summer in both years of the study. In addition, infection significantly reduced psi(L) and g(s) in the most basal leaf positions in late summer in both years. Whole shoot hydraulic conductance was reduced by both low water and infection treatments. However, per cent embolized vessels and mean vessel diameter were affected by drought treatment only. These results imply that the major effect of infection by X. fastidiosa occurs due to reduced hydraulic conductance caused by clogging of the vessels, and not increased cavitation and embolism of xylem elements. The reduced K(h) caused by X. fastidiosa infection acts additively with the water limitation imposed by Drought stress.     

Vulnerability to cavitation in populations of two desert species, Hymenoclea salsola and Ambrosia dumosa, from different climatic regions

Seeds from different populations of two desert species, Hymenocleasalsola Torr. and A. Gray and Ambrosia dumosa (A. Gray) Payne,were collected along a climatic gradient, germinated in a greenhouseand the plants tested for their vulnerability to cavitationby the air-pressure method. Differences among populations wereevident in A. dumosa, but not in H. salsola. Greenhouse treatmentssimulating regimes in temperature and relative humidity encounteredin different desert environments did not cause appreciable changesin vulnerability to cavitation. It is suggested that a homeostaticmechanism may have helped in maintaining a constant water potentialdrop in the xylem with little need for an adjustment in theresistance to cavitation. Different plant organs had differentvulnerabilities to cavitation, with roots being the most andwoody stems the least susceptible. Young green twigs were intermediate.A simulation model confirmed that low water potentials are mostlikely to cause runaway cavitation in the roots, not in theother organs. It is hypothesized that green twigs are adaptedto the favourable water conditions of the growing season, whilewoody stems are adapted to endure prolonged periods of droughtstress. Key words: Cavitation, xylem embolism, hydraulic conductance, Hymenoclea salsola, Ambrosia dumosa     

Stomatal factors and vulnerability of stem xylem to cavitation in poplars

The relationships between the vulnerability of stem xylem to cavitation, stomatal conductance, stomatal density, and leaf and stem water potential were examined in six hybrid poplar (P38P38, Walker, Okanese, Northwest, Assiniboine and Berlin) and balsam poplar (Populus balsamifera) clones. Stem xylem cavitation resistance was examined with the Cavitron technique in well-watered plants grown in the greenhouse. To investigate stomatal responses to drought, plants were subjected to drought stress by withholding watering for 5 (mild drought) and 7 (severe drought) days and to stress recovery by rewatering severely stressed plants for 30 min and 2 days. The clones varied in stomatal sensitivity to drought and vulnerability to stem xylem cavitation. P38P38 reduced stomatal conductance in response to mild stress while the balsam poplar clone maintained high leaf stomatal conductance under more severe drought stress conditions. Differences between the severely stressed clones were also observed in leaf water potentials with no or relatively small decreases in Assiniboine, P38P38, Okanese and Walker. Vulnerability to drought-induced stem xylem embolism revealed that balsam poplar and Northwest clones reached loss of conductivity at lower stem water potentials compared with the remaining clones. There was a strong link between stem xylem resistance to cavitation and stomatal responsiveness to drought stress in balsam poplar and P38P38. However, the differences in stomatal responsiveness to mild drought suggest that other drought-resistant strategies may also play a key role in some clones of poplars exposed to drought stress.     

Three Different Methods for Measuring Xylem Cavitation and Embolism: A Comparison

Three different methods for measuring xylem embolism due towater cavitation were compared—the acoustic method, thehydraulic method and the anatomical method. Young plants ofCeratonia siliqua L. were water stressed for 9, 16 and 23 d. Xylem cavitation was detected by counting ultrasound (100–300kHz) acoustic emissions (AE) from 1-year-old twigs (acousticmethod). Xylem embolism was detected by measuring the loss ofhydraulic conductivity of twigs of the same age (hydraulic method).The blockage of single xylem conduits was detected by perfusingSafranin into the xylem of 1-year-old twigs of stressed plantsand measuring the number and the diameters of non-conductingxylem conduits, under the microscope (anatomical method). It was noted that: (a) the number of AE and the loss of conductivityincreased with the water stress applied; (b) a linear relationseemed to exist between the number of AE and the loss of conductivity,suggesting that the AE counted could be only (or mainly) producedin the xylem conduits; (c) the vulnerability of the xylem conduitsto embolism was a direct function of their diameter; and (d)the measured loss of conductivity was of the same order of magnitudeas the theoretical one. The three methods gave fairly similar results. Nonetheless,they are not alternative to one another in that: (a) the acousticmethod allows continuous recordings to be made but does notprovide information about the actual damage suffered by plants;(b) the hydraulic method is very informative but destructive;and (c) the anatomical method is very useful both in phytogeographicaland in genetic improvement studies. Ceratonia siliqua L, Carob tree, water stress, xylem embolism, acoustic method, hydraulic method, anatomical method     

Three Different Methods for Measuring Xylem Cavitation and Embolism: A Comparison

Three different methods for measuring xylem embolism due towater cavitation were compared—the acoustic method, thehydraulic method and the anatomical method. Young plants ofCeratonia siliqua L. were water stressed for 9, 16 and 23 d. Xylem cavitation was detected by counting ultrasound (100–300kHz) acoustic emissions (AE) from 1-year-old twigs (acousticmethod). Xylem embolism was detected by measuring the loss ofhydraulic conductivity of twigs of the same age (hydraulic method).The blockage of single xylem conduits was detected by perfusingSafranin into the xylem of 1-year-old twigs of stressed plantsand measuring the number and the diameters of non-conductingxylem conduits, under the microscope (anatomical method). It was noted that: (a) the number of AE and the loss of conductivityincreased with the water stress applied; (b) a linear relationseemed to exist between the number of AE and the loss of conductivity,suggesting that the AE counted could be only (or mainly) producedin the xylem conduits; (c) the vulnerability of the xylem conduitsto embolism was a direct function of their diameter; and (d)the measured loss of conductivity was of the same order of magnitudeas the theoretical one. The three methods gave fairly similar results. Nonetheless,they are not alternative to one another in that: (a) the acousticmethod allows continuous recordings to be made but does notprovide information about the actual damage suffered by plants;(b) the hydraulic method is very informative but destructive;and (c) the anatomical method is very useful both in phytogcographicaland in genetic improvement studies. Ceratonia siliqua L., Carob tree, water stress, xylem embolism, acoustic method, hydraulic method, anatomical method     

Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas)

The impact of water deficit on stomatal conductance (g(s)), petiole hydraulic conductance (K(petiole)), and vulnerability to cavitation (PLC, percentage loss of hydraulic conductivity) in leaf petioles has been observed on field-grown vines (Vitis vinifera L. cv. Chasselas). Petioles were highly vulnerable to cavitation, with a 50% loss of hydraulic conductivity at a stem xylem water potential (Ψ(x)) of -0.95?MPa, and up to 90% loss of conductivity at a Ψ(x) of -1.5?MPa. K(petiole) described a daily cycle, decreasing during the day as water stress and evapotranspiration increased, then rising again in the early evening up to the previous morning's K(petiole) levels. In water-stressed vines, PLC increased sharply during the daytime and reached maximum values (70-90%) in the middle of the afternoon. Embolism repair occurred in petioles from the end of the day through the night. Indeed, PLC decreased in darkness in water-stressed vines. PLC variation in irrigated plants showed the same tendency, but with a smaller amplitude. The Chasselas cultivar appears to develop hydraulic segmentation, in which petiole cavitation plays an important role as a 'hydraulic fuse', thereby limiting leaf transpiration and the propagation of embolism and preserving the integrity of other organs (shoots and roots) during water stress. In the present study, progressive stomatal closure responded to a decrease in K(petiole) and an increase in cavitation events. Almost total closure of stomata (90%) was measured when PLC in petioles reached >90%.     

Vulnerability of xylem vessels to cavitation in sugar maple. Scaling from individual vessels to whole branches

The relation between xylem vessel age and vulnerability to cavitation of sugar maple (Acer saccharum Marsh.) was quantified by measuring the pressure required to force air across bordered pit membranes separating individual xylem vessels. We found that the bordered pit membranes of vessels located in current year xylem could withstand greater applied gas pressures (3.8 MPa) compared with bordered pit membranes in vessels located in older annular rings (2.0 MPa). A longitudinal transect along 6-year-old branches indicated that the pressure required to push gas across bordered pit membranes of current year xylem did not vary with distance from the growing tip. To understand the contribution of age-related changes in vulnerability to the overall resistance to cavitation, we combined data on the pressure thresholds of individual xylem vessels with measurements of the relative flow rate through each annual ring. The annual ring of the current year contributed only 16% of the total flow measured on 10-cm-long segments cut from 6-year-old branches, but it contributed more than 70% of the total flow when measured through 6-year-old branches to the point of leaf attachment. The vulnerability curve calculated using relative flow rates measured on branch segments were similar to vulnerability curves measured on 6-year-old branches (pressure that reduces hydraulic conductance by 50% = 1.6-2.4 MPa), whereas the vulnerability curve calculated using relative flow rates measured on 6-year-old branches were similar to ones measured on the extension growth of the current year (pressure that reduces hydraulic conductance by 50% = 3.8 MPa). These data suggest that, in sugar maple, the xylem of the current year can withstand larger xylem tensions than older wood and dominates water delivery to leaves.     

Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange

In woody plants, photosynthetic capacity is closely linked to rates at which the plant hydraulic system can supply water to the leaf surface. Drought‐induced embolism can cause sharp declines in xylem hydraulic conductivity that coincide with stomatal closure and reduced photosynthesis. Recovery of photosynthetic capacity after drought is dependent on restored xylem function, although few data exist to elucidate this coordination. We examined the dynamics of leaf gas exchange and xylem function in Eucalyptus pauciflora seedlings exposed to a cycle of severe water stress and recovery after re‐watering. Stomatal closure and leaf turgor loss occurred at water potentials that delayed the extensive spread of embolism through the stem xylem. Stem hydraulic conductance recovered to control levels within 6 h after re‐watering despite a severe drought treatment, suggesting an active mechanism embolism repair. However, stomatal conductance did not recover after 10 d of re‐watering, effecting tighter control of transpiration post drought. The dynamics of recovery suggest that a combination of hydraulic and non‐hydraulic factors influenced stomatal behaviour post drought.     

Xylem Hydraulic Characteristics, Water Relations and Wood Anatomy of the Resurrection PlantMyrothamnus flabellifoliusWelw.

Myrothamnus flabellifoliusWelw. is a desiccation-tolerant (‘resurrection’)plant with a woody stem. Xylem vessels are narrow (14 µmmean diameter) and perforation plates are reticulate. This leadsto specific and leaf specific hydraulic conductivities thatare amongst the lowest recorded for angiosperms (k_s0.87 kg m^-1MPa^-1s^-1;k_l3.28x10^-5kg m^-1MPa^-1s^-1, stem diameter 3 mm). Hydraulic conductivitiesdecrease with increasing pressure gradient. Transpiration ratesin well watered plants were moderate to low, generating xylemwater potentials of -1 to -2 MPa. Acoustic emissions indicatedextensive cavitation events that were initiated at xylem waterpotentials of -2 to -3 MPa. The desiccation-tolerant natureof the tissue permits this species to survive this interruptionof the water supply. On rewatering the roots pressures thatwere developed were low (2.4 kPa). However capillary forceswere demonstrated to be adequate to account for the refillingof xylem vessels and re-establishment of hydraulic continuityeven when water was under a tension of -8 kPa. During dehydrationand rehydration cycles stems showed considerable shrinking andswelling. Unusual knob-like structures of unknown chemical compositionwere observed on the outer surface of xylem vessels. These maybe related to the ability of the stem to withstand the mechanicalstresses associated with this shrinkage and swelling.Copyright1998 Annals of Botany Company cavitation, desiccation, hydraulic conductivity, refilling, resurrection plant, root pressure, xylem anatomy,Myrothamnus flabellifolius