Modelling the impact of heterogeneous rootzone water distribution on the regulation of transpiration by hormone transport and/or hydraulic pressures

Aims

A simulation model to demonstrate that soil water potential can regulate transpiration, by influencing leaf water potential and/or inducing root production of chemical signals that are transported to the leaves.

Methods

Signalling impacts on the relationship between soil water potential and transpiration were simulated by coupling a 3D model for water flow in soil, into and through roots (Javaux et al. 2008) with a model for xylem transport of chemicals (produced as a function of local root water potential). Stomatal conductance was regulated by simulated leaf water potential (H) and/or foliar chemical signal concentrations (C; H?+?C). Split-root experiments were simulated by varying transpiration demands and irrigation placement.

Results

While regulation of stomatal conductance by chemical transport was unstable and oscillatory, simulated transpiration over time and root water uptake from the two soil compartments were similar for both H and H?+?C regulation. Increased stomatal sensitivity more strongly decreased transpiration, and decreased threshold root water potential (below which a chemical signal is produced) delayed transpiration reduction.

Conclusions

Although simulations with H?+?C regulation qualitatively reproduced transpiration of plants exposed to partial rootzone drying (PRD), long-term effects seemed negligible. Moreover, most transpiration responses to PRD could be explained by hydraulic signalling alone.     

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.     

Detection of black-foot and Petri disease pathogens in soils of grapevine nurseries and vineyards using bait plants

Background and aims

Little information is currently available regarding the number of species of black-foot and Petri disease pathogens present in soil and their capacity to infect grapevine roots and reach the xylem vessels.

Methods

Seedlings of grapevine rootstock 41-B, and cvs. Bobal and Palomino were planted both in pots containing soil samples collected from commercial vineyards and in nursery fields. Roots and xylem vessels were later analyzed for fungal isolation.

Results

Black-foot pathogens: Ilyonectria alcacerensis, I. macrodidyma, I. novozelandica and I. torresensis were frequently isolated from roots of seedlings grown in all soils evaluated, whereas Petri disease pathogens: Cadophora luteo-olivacea, Phaeoacremonium aleophilum, Pm. parasiticum and Phaeomoniella chlamydospora were only isolated from xylem vessels of seedlings grown in nursery soils, with a low incidence. Ilyonectria alcacerensis, I. novozelandica and I. torresensis were isolated for the first time from grapevines in Spain, and Pm. parasiticum and Ca. luteo-olivacea were detected for the first time in nursery soils.

Conclusions

Our results confirm nursery and vineyard soils as an important inoculum source for black-foot pathogens and demonstrate the presence of several Petri disease pathogens in nursery soils.     

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.     

Signalling mechanisms involved in the response of two varieties of Humulus lupulus L. to soil drying: I. changes in xylem sap pH and the concentrations of abscisic acid and anions

Background and aims

Soil drying leads to the generation of chemical signals in plants that regulate water use via control of the stomatal aperture. The aim of our work was to identify the presence and identity of potential chemical signals, their dynamics, and their relationship with transpiration rate during soil drying in hop (Humulus lupulus (L.)) plants.

Methods

We used pressure chamber technique for measurement of shoot water potential and collection of shoot xylem sap. We analyzed concentrations of abscisic acid (ABA), nitrate, phosphate, sulphate and malate in sap and also the rate of whole plant transpiration.

Results

Transpiration rate decreased prior to changes in shoot water potential. The concentration of ABA in xylem sap continuously increased from early to later stages of water stress, whereas in leaves it increased only at later stages. Shoot sap pH increased simultaneously with the decrease of transpiration rate. Xylem sap alkalization was in some cases accompanied by a decrease in nitrate concentration and an increase in malate concentration. Concentration of sulphate increased in xylem sap during drying and sulphate in combination with a higher ABA concentration enhanced stomatal closure.

Conclusions

Several early chemical signals appear in sap of hop plants during soil drying and their impact on transpiration may vary according to the stage of soil drying.     

Function and structure of leaves contributing to increasing water storage with height in the tallest <Emphasis Type="Italic">Cryptomeria japonica</Emphasis> trees of Japan

Key message

In Cryptomeria japonica , transfusion tissue in leaves may have functions of water storage and supply, which could compensate for hydraulic constraints with increasing height.

Abstract

The tallest trees of Cryptomeria japonica occur in climatic regions similar to the world’s tallest trees. We hypothesized that tall C. japonica trees would have evolved adaptive mechanisms to overcome height growth limitation. Here, we focused on foliar water storage, a mechanism recently discovered in Sequoia sempervirens. In C. japonica, leaf water potential at turgor loss did not change with height or light availability, while leaf hydraulic capacitance and succulence (water content per leaf surface area) increased, suggesting hydraulic compensation. Plasticity of leaf morphology could contribute to avoiding negative effects of height on photosynthesis. We also focused on the structure and function of transfusion tissue in leaves and its role in water storage and supply. Cross-sectional area of transfusion tissue increased with height, whereas that of xylem was constant. We confirmed that water flowed from vascular bundle to mesophyll via the transfusion tissue. Cryo-scanning electron microscopy images of leaf cross sections showed that transfusion cells were flattened, but not fully dehydrated when leaf water potential decreased in situ and by experimental dehydration, and cell deformation was more marked for treetop leaves than for lower-crown leaves. The shape of transfusion cells recovered at predawn as well as after experimental rehydration. As in S. sempervirens, transfusion tissue of C. japonica may function as a hydraulic buffer, absorbing and releasing water according to leaf water status. Anatomical and hydraulic properties contributing to foliar water storage may be an adaptive mechanism acquired by tall Cupressaceae trees to overcome the hydraulic constraints on physiological function with increasing height.

     

Changes in soil hyphal abundance and viability can alter the patterns of hydraulic redistribution by plant roots

Background and aims

We conducted a mesocosm study to investigate the extent to which the process of hydraulic redistribution of soil water by plant roots is affected by mycorrhizosphere disturbance.

Methods

We used deuterium-labeled water to track the transfer of hydraulically lifted water (HLW) from well-hydrated donor oaks (Quercus agrifolia Nee.) to drought-stressed receiver seedlings growing together in mycorrhizal or fungicide-treated mesocosms. We hypothesized that the transfer of HLW from donor to receiver plants would be enhanced in undisturbed (non-fungicide-treated) mesocosms where an intact mycorrhizal hyphal network was present.

Results

Contrary to expectations, both upper soil and receiver seedlings contained significantly greater proportions of HLW in mesocosms where the abundance of mycorrhizal hyphal links between donor and receiver roots had been sharply reduced by fungicide application. Reduced soil hyphal density and viability likely hampered soil moisture retention properties in fungicide-treated mesocosms, thus leading to faster soil water depletion in upper compartments. The resulting steeper soil water potential gradient between taproot and upper compartments enhanced hydraulic redistribution in fungicide-treated mesocosms.

Conclusions

Belowground disturbances that reduce soil hyphal density and viability in the mycorrhizosphere can alter the patterns of hydraulic redistribution by roots through effects on soil hydraulic properties.     

Strong hydraulic segmentation and leaf senescence due to dehydration may trigger die-back in Nothofagus dombeyi under severe droughts: a comparison with the co-occurring Austrocedrus chilensis

Key message

Total leaf hydraulic dysfunction during severe drought could lead to die-back in N. dombeyi , while hydraulic traits of A. chilensis allow it to operate far from the threshold of total hydraulic failure.

Abstract

Die-back was observed in South America temperate forests during one of the most severe droughts of the 20th century (1998–1999). During this drought Austrocedrus chilensis trees survived, whereas trees of the co-occurring species (Nothofagus dombeyi) experienced symptoms of water stress, such as leaf wilting and abscission, before tree die-back occurred. We compared hydraulic traits of these two species (a conifer and an angiosperm species, respectively) in a forest stand located close to the region with records of N. dombeyi mass mortality. We asked whether different hydraulic traits exhibited by the two species could help explain their contrasting survivorship rates. Austrocedrus chilensis had wide leaf safety margins, which appear to be the consequence of relatively high leaf-and-stem capacitance, large stored water use, strong stomatal control and ability to recover from embolism-induced loss of leaf hydraulic capacity. On the other hand, N. dombeyi even though had a stem hydraulic threshold of ?6.7 MPa before reaching substantial hydraulic failure (P₈₈), leaf P₈₈ occurred at leaf water potentials of only ?2 MPa, which probably are reached during anomalous droughts. Massive mortality in N. dombeyi appears to be the result of the total loss of leaf hydraulic conductance leading to leaf dehydration and leaf drop. Drought occurs during the summer and it is highly likely that N. dombeyi cannot recover its photosynthetic surface to produce carbohydrates required to avoid tissue injury in the winter season with subfreezing temperatures. Strong hydraulic segmentation in N. dombeyi does not seem to have an adaptive value to survive severe droughts.     

Xylem sap calcium concentrations do not explain liming-induced inhibition of legume gas exchange

Background and aims

Liming is considered normal agricultural practise for remediating soil acidity and improving crop productivity; however recommended lime applications can reduce yield. We tested the hypothesis that elevated xylem sap Ca²⁺ limited gas exchange of Phaseolus vulgaris L. and Pisum sativum L. plants that exhibited reduced shoot biomass and leaf area when limed.

Methods

We used Scholander and whole-plant pressure chamber techniques to collect root and leaf xylem sap, a calcium-specific ion-selective electrode to measure xylem sap Ca²⁺, infra-red gas analysis to measure gas exchange of limed and unlimed (control) plants, and a detached leaf transpiration bioassay to determine stomatal sensitivity to Ca²⁺.

Results

Liming reduced shoot biomass, leaf area and leaf gas exchange in both species. Root xylem sap Ca²⁺ concentration was only increased in P. vulgaris and not in P. sativum. Detached leaves of both species required 5 mM Ca²⁺ supplied to via the transpiration stream to induce stomatal closure, however, maximum in vivo xylem sap Ca²⁺ concentrations of limed plants was only 1.7 mM and thus not high enough to influence stomata.

Conclusion

We conclude that an alternative xylem-borne antitranspirant other than Ca²⁺ decreases gas exchange of limed plants.     

Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate

Background and aims

Iron (Fe) deficiency chlorosis associated with high levels of soil bicarbonate is one of the main nutritional disorders observed in sensitive grapevine genotypes. The aim of the experiment was to assess both the independent and combined effects of Fe and bicarbonate nutrition in grapevine.

Methods

Plants of the Fe chlorosis tolerant 140 Ruggeri rootstock were grown with and without Fe(III)-EDTA and bicarbonate in the nutrient solution. SPAD index, plant growth, root enzyme (PEPC, MDH, CS, NADP⁺ ?IDH) activities, kinetic properties of root PEPC, organic acid concentrations in roots and xylem sap and xylem sap pH were determined. A factorial statistical design with two factors (Fe and BIC) and two levels of each factor was adopted: +Fe and ?Fe, and +BIC and ?BIC.

Results

This rootstock strongly reacted to Fe deficiency by activating several response mechanisms at different physiological levels. The presence of bicarbonate in the nutrient solution changed the activity of PEPC and TCA related enzymes (CS, NADP⁺-IDH) and the accumulation/translocation of organic acids in roots of Fe-deprived plants. Moreover, this genotype increased root biomass and root malic acid concentration in response to high bicarbonate levels in the substrate. Bicarbonate also enhanced leaf chlorophyll content.

Conclusions

Along with a clear independent effect on Fe nutrition, our data support a modulating role of bicarbonate on Fe deficiency response mechanisms at root level.     

Uptake of water from a Kandosol subsoil. II. Control of water uptake by roots

Aim

To test for the presence of an impediment to water flow at the soil-root interface.

Methods

Wheat plants were grown in repacked and undisturbed field soil. Their transpiration rate, E, was varied in several steps from low to high and then back to low again, while the hydrostatic pressure in the leaf xylem, ψ _xylem, was measured non-destructively and continuously. These measurements were compared to a mathematical model that calculated ψ _xylem by assuming that the hydraulic resistance across the plant was constant and that the radial flow of water to unit length of a typical plant root generated gradients in pressure in the soil water.

Results

For the repacked soil, the radial flow model could not match the experiment during the falling phase of E, unless it was assumed that either an additional, constant, interfacial resistance between the soil and the roots had developed when E was large and ψ _xylem was rapidly falling, or that the resistance within the plant had changed. For the undisturbed field soil, the radial flow model did not agree with the experiment. Plausible agreement was achieved when plant water uptake was accounted for using a distributed sink model in HYDRUS-1D, with E integrated across the rootzone. This approach was based on the measured large variation in the vertical distribution of roots.

Conclusions

There was no strong evidence of large drawdowns of soil water in the rhizosphere, even when ψ _xylem was falling rapidly when E was large and the soil was moderately dry. Thus, there seems to have been an additional impediment to water flow from soil to plant, either within the plant, or at the interface between the two.     

Hydraulic properties of European elms: xylem safety-efficiency tradeoff and species distribution in the Iberian Peninsula

Key message

Ulmus minor and U. glabra show a trade-off between safety and efficiency in water transport, and U. laevis shows adaptations to waterlogged environments.

Abstract

Three native elm species grow in Europe: Ulmus minor Mill., U. glabra Huds. and U. laevis Pall., and within the Iberian Peninsula their habitats mainly differ in water availability. We evaluated firstly whether vulnerability to xylem embolism caused by water-stress has been a determinant factor affecting their distribution; secondly, if their xylem anatomy differs due to water availability dissimilarities; and thirdly, if these species present a trade-off between water transport safety and efficiency. Plants of the three species were grown in a common-garden in Madrid, Central Spain. The centrifuge method was used for constructing the vulnerability curves, and anatomical measurements were carried out with an optical microscope. We found clear differences in conductivity and cavitation vulnerability between the three species. Although all three elms were highly vulnerable to cavitation, U. minor was significantly more resistant to water stress cavitation. This species reached 50 % loss in conductivity at ?1.1 MPa, compared to U. glabra that did so at ?0.5 MPa, and U. laevis at ?0.4 MPa. Maximum xylem specific conductivity and maximum leaf specific conductivity were two to three times higher in U. glabra when compared to U. minor. A clear trade-off between safety against losses of conductivity and water transport efficiency was observed considering both U. minor and U. glabra samples. Ulmus minor’s hydraulic configuration was better adapted to overcome drought episodes. The expected aridification of the Iberian Peninsula could compromise Ulmus populations due to their high vulnerability to drought stress.     

Comparative axial widening of phloem and xylem conduits in small woody plants

Key message

Along the stem axis phloem’s sieve elements increase in diameter basally at rates comparable to those of xylem conduits and in agreement with principles of hydraulic optimization.

Abstract

Plant physiology relies on the efficiency of the two long-distance transport systems of xylem and phloem. Xylem architecture comprises conduits of small dimensions towards the stem apex, where transpiration-induced tensions are the highest along the root-to-leaves hydraulic pathway, and widen basally to minimize the path length resistance to water flow. Instead, information on phloem anatomy and allometry is extremely scarce, although potentially relevant for the efficiency of sugar transportation. We measured the hydraulic diameter (Dh) of both xylem conduits and phloem sieve elements in parallel at different heights along the stem of a small tree of Picea abies, Fraxinus excelsior and Salix eleagnos. Dh increased from the stem apex to base in both xylem and phloem, with a higher scaling exponent (b) of sieve elements than that of tracheids in the conifer (0.19 vs. 0.14) and lower than that of vessels in the angiosperms (0.14–0.22 vs. 0.19–0.40). In addition, sieve elements were larger than tracheids in P. abies and narrower than angiosperms vessels at any height along the stem. In conclusion, axial conduit widening would seem to be a key feature of both xylem and phloem long-distance transport architectures.     

Conservation of functional traits leads to shrub expansion across a chronosequence of shrub thicket development

Key message

Robust physiology of Myrica cerifera across a chronosequence (i.e., space for time substitution) of shrub thicket age classes contributes to rapid cover expansion observed in the last 50 years.

Abstract

Many studies have documented the causes of woody expansion into grasslands, but few address unique morphological and physiological traits that facilitate expansion. Myrica cerifera, an evergreen N-fixer, is the dominant shrub on many barrier islands of the southeastern United States. Cover of Myrica cerifera has expanded by ~400 % on Hog Island, Virginia, in the past 50 years. Accretion of the northern end of the island has resulted in a chronosequence (i.e., space for time substitution) of both soil age and shrub thicket development. We investigated functional traits and physiological parameters related to light capture, processing and water balance of M. cerifera across shrub thickets of four age classes from ~10 to ~50 years. We hypothesized that light processing capabilities and hydraulic capacity would be reduced with thicket age. Spatial variation in morphology (i.e., leaf thickness, leaf area) and structure (i.e., leaf angle) related to light capture was observed. Yet, little or no differences were detected in stomatal density, photosynthetic pigments, electron transport rate (ETR) and hydraulic conductivity across sites. Previous research has shown declines in leaf N content, productivity and leaf litter production across the chronosequence. In contrast, we observed that physiology remains consistent despite considerable differences in thicket age and development. Myrica cerifera maintains high photosynthetic and hydraulic efficiency, factors which enable expansion and maintenance of shrub thickets in mesic coastal environments.     

Non-invasive pressure probes magnetically clamped to leaves to monitor the water status of wheat

Background and aims

Being able to monitor the hydration status of a plant would be useful to breeding programs and to providing insight into adaptation to water-limited environments, but most current methods are destructive or laborious. We evaluated novel non-invasive pressure probes (commercial name: ZIM-probe) for their potential in monitoring the water status of wheat (Triticum aestivum L.) leaves.

Methods

The probes consist of miniature pressure sensors that clamp to the leaves via magnets and detect relative changes in hydration status. Probes were clamped to leaves of six individual plants of the cultivar Wyalkatchem at the stem elongation stage and compared against traditional plant water relations measurements.

Results

Output from the probes, called patch-pressure (P _p ), correlated well with leaf water potential and transpiration of individual plants. Variation between plants in the original clamp pressure exerted by the magnets and leaf individual properties led to variations in the amplitude of the diurnal P _p profiles, but not in the kinetics of the curves where P _p responded simultaneously in all plants to changes in the ambient environment (light and temperature).

Conclusions

Drying and rewatering cycles and analysis of the curve kinetics identified several methods that can be used to test comparisons of water status monitoring of wheat genotypes under water deficit.     

Vascular Function in Grape Berries across Development and Its Relevance to Apparent Hydraulic Isolation

During the latter stages of development in fleshy fruit, water flow through the xylem declines markedly and the requirements of transpiration and further expansion are fulfilled primarily by the phloem. We evaluated the hypothesis that cessation of water transport through the xylem results from disruption or occlusion of pedicel and berry xylem conduits (hydraulic isolation). Xylem hydraulic resistance (R_h) was measured in developing fruit of grape (Vitis vinifera ‘Chardonnay’) 20 to 100 d after anthesis (DAA) and compared with observations of xylem anatomy by light and cryo-scanning electron microscopy and expression of six plasma membrane intrinsic protein (PIP) aquaporin genes (VvPIP1;1, VvPIP1;2, VvPIP1;3, VvPIP2;1, VvPIP2;2, VvPIP2;3). There was a significant increase in whole berry R_h and receptacle R_h in the latter stages of ripening (80–100 DAA), which was associated with deposition of gels or solutes in many receptacle xylem conduits. Peaks in the expression of some aquaporin isoforms corresponded to lower whole berry R_h 60 to 80 DAA, and the increase in R_h beginning at 80 DAA correlated with decreases in the expression of the two most predominantly expressed PIP genes. Although significant, the increase in berry R_h was not great enough, and occurred too late in development, to explain the decline in xylem flow that occurs at 60 to 75 DAA. The evidence suggests that the fruit is not hydraulically isolated from the parent plant by xylem occlusion but, rather, is “hydraulically buffered” by water delivered via the phloem.The development of grape (Vitis vinifera) berries is typical of many fleshy fruits, following a double sigmoid pattern of growth with three distinct phases: an initial phase of rapid cell division and expansion in green berries, a short transitory phase of very little growth, and a final phase in which growth is reinitiated and the fruit ripens. The transition to the ripening phase is accompanied by many physiological changes, such as the production of anthocyanins and fruit softening. In grape, these distinctive and highly visible physiological changes are collectively referred to as veraison. The rapid accumulation of sugars that is initiated in the berry mesocarp around the time of veraison is accompanied by a dramatic shift in the proportion of xylem and phloem transport (Lang and Thorpe, 1989; Greenspan et al., 1994, 1996). This same shift, albeit more gradual, occurs in many other fleshy fruits such as tomato (Solanum lycopersicum; Ho et al., 1987), apple (Malus domestica; Lang and Ryan, 1994; Drazeta et al., 2004), and kiwifruit (Actinidia deliciosa; Dichio et al., 2003) as well as in the flowers of tropical trees (Chapotin et al., 2003). The sudden reduction in xylem transport to the fruit is perceived as a mechanism to hydraulically isolate the fruit and buffer them from environmental stresses experienced by the parent plant.Using mass balance techniques, Greenspan et al. (1994, 1996) reported major changes in the role of the xylem and phloem in water transport to the grape berry at veraison. During the first growth phase, the xylem provides the majority of water transport into the berry. In the final growth stage, the phloem provides more than 80% of the berry''s water requirements and the contribution of the xylem becomes negligible. Berry water status also becomes apparently uncoupled from plant water status after veraison. Before veraison, diurnal contractions in berry diameter were strongly related to changes in plant (stem) water potential, while after veraison, diurnal contractions were greatly reduced and unrelated to changes in stem water potential (Matthews and Shackel, 2005). A similar lack of response was also observed for mesocarp cell turgor after veraison (Thomas et al., 2006). Thus, it is clear that some mechanism acts to decouple berry water relations from the water status of the parent plant.Over the past two decades, a general consensus has developed that the berry xylem becomes physically disrupted after veraison, effectively blocking the xylem pathway and isolating the fruit essentially as a whole from the parent plant (During et al., 1987; Findlay et al., 1987; Lang and Ryan, 1994). Evidence for this has been provided by observations of dye uptake into the berry through the xylem. When the cut pedicel of a preveraison berry is submerged in dye, the dye is taken up into peripheral and axial xylem conduits of the entire berry (Findlay et al., 1987; Creasy et al., 1993; Rogiers et al., 2001). After veraison, dye uptake is limited to the base of the berry vasculature (brush). From this evidence, together with micrographs that appeared to show stretched and ruptured xylem conduits in postveraison berries, it was inferred that the lignified tracheids present at veraison were physically torn apart by the expansion of the berry that occurred postveraison.Recent experimental work using a range of techniques suggests that the hypothesis of physical disruption may be oversimplified and that the berry xylem remains at least potentially functional after veraison (Bondada et al., 2005; Keller et al., 2006; Chatelet et al., 2008b). The results of Chatelet et al. (2008a, 2008b) demonstrate that the majority of xylem conduits in the berry remain intact after veraison and suggest that xylem development (growth of new conduits) continues well into the postveraison growth phase. Using both a modified pressure plate/membrane apparatus and a wicking technique, it was demonstrated that dye moved through the xylem of postveraison berries when a hydrostatic pressure or matric gradient was applied between the pedicel and the cut stylar surface (Bondada et al., 2005; Chatelet et al., 2008b). Keller et al. (2006) demonstrated this in reverse, showing that berry xylem was still capable of conducting a dye tracer back to the parent plant if the dye was introduced at the cut stylar end while the plant was transpiring. Thus, given a large enough pressure gradient, the xylem of postveraison berries retains the potential to transport water between the parent plant and the berry or vice versa. However, anatomical measurements and dye tracer studies can only be used to infer the degree to which fruit may become isolated from the parent plant. Knowledge of changes in hydraulic resistance (R_h) is required to determine whether xylem dysfunction is actually responsible for declining xylem flows reported with the progression of ripening. It is also important to differentiate between xylem flows and R_h, as these variables are sometimes confused in the literature; xylem flow rates can vary independently of R_h if water potential gradients along the pathway are altered.Previous studies examining changes in R_h associated with the development of fleshy fruit generally indicate that R_h increases during ripening but show differences in the timing and location of the increase. Some fruits develop an abscission zone in the pedicel or receptacle that is associated with vascular constriction and high R_h (Mackenzie, 1988; Lee, 1989; Van Ieperen et al., 2003). However, although some table grapes are believed to develop an abscission zone, there is no evidence of an abscission zone in wine grapes (Pratt, 1971). Tyerman et al. (2004) reported a substantial increase in R_h of grape berries after veraison, although this increase in resistance did not occur in the pedicel or receptacle but mainly in the distal section of the berries. Similarly, Malone and Andrews (2001) evaluated R_h in developing tomato fruits and stems and found that R_h increased in the fruit, but not proximal to the calyx. In apple, Lang and Ryan (1994) observed an increase in R_h at 80 d after anthesis (DAA) and also reported an increasing proportion of samples in which the xylem was completely occluded with age. Although they described these data as pedicel R_h, their measurements actually included the fruit vascular pathway; therefore, it is difficult to determine if the increase in R_h was manifested in the fruit or the pedicel.Increases in pedicel and receptacle R_h should be associated with changes in the dimensions or conductive state or xylem conduits. An increase in the R_h within the fruit may relate either to xylem dysfunction or to extravascular resistance beyond the xylem. Although they were not able to partition an increase in fruit R_h between the apoplast and symplast, Tyerman et al. (2004) suggested that the site of increased resistance may be the plasma membranes of vascular parenchyma cells separating xylem conduits and mesocarp cells rather than the xylem itself. A likely candidate driving hydraulic isolation at the cellular level is changes in plasma membrane R_h resulting from the differential expression and activity of aquaporins. Aquaporins are a family of transmembrane proteins considered to be largely responsible for the high permeability to water exhibited by plasma membranes. The regulation of R_h by aquaporins is now well documented in roots (Martre et al., 2001; McElrone et al., 2007; Vandeleur et al., 2009), and oxidative gating of aquaporins has been reported to reduce hydraulic conductivity by 90% in cells of the giant algae Chara (Henzler et al., 2004). The results of previous work suggest that aquaporins play an important role in the regulation of water movement during the development of flowers, seeds, and fruits (Maurel et al., 1995; Gao et al., 1999; Picaud et al., 2003; Shiota et al., 2006; Zhou et al., 2007). Changes in the expression of the plasma membrane intrinsic protein (PIP) PIP1 and PIP2 aquaporin gene families have been noted in ripening grapes (Picaud et al., 2003; Fei et al., 2004), although the effects of these changes on water transport (membrane conductivity) have not been documented. An increase of R_h between the mesocarp cells and the xylem within the fruit could provide a mechanism to restrict water movement between the parent plant and the berry if a large gradient in xylem tension existed between the two (Tyerman et al., 2004).While the concept of hydraulic isolation is generally accepted as part of the physiology of fleshy fruit development, we note that no studies have demonstrated an increase in R_h that is coincident with the decline in xylem flow. Additionally, measured variation in the R_h of the fruit and pedicel has not been quantitatively related to the water requirements of the fruit, taking into account water potential gradients between the fruit and the parent plant. In this study, we examined changes in the R_h of the berry, receptacle, and pedicel of Chardonnay grape over the course of fruit development. These measurements were compared against observations of xylem anatomy and aquaporin gene expression in order to investigate the hypotheses that (1) occlusion and/or disruption of xylem conduits results in the hydraulic isolation of ripening grape berries, and (2) an increase in the R_h of the berry is associated with changes in the expression of aquaporin genes in the mesocarp.     

Comment on: “neutron imaging reveals internal plant water dynamics”

Introduction

In a recent paper, Warren et al. (2013) illustrated the potential of neutron radiography to visualize water dynamics in soil and plants.

Methods

After injection of deuterated water (D₂O) in soil, the authors could monitor the changes of D₂O concentration in roots.

Results

Based on the radiographs, the authors concluded that D₂O was transported from roots growing in a wet soil region to roots in a dry region, proving hydraulic redistribution between roots. However, this interpretation depends on the correct estimation of D₂O concentration in soil.

Conclusions

The experiments of Warren et al. (2013) could also be explained by diffusion of D₂O from soil to roots, without hydraulic redistribution within the root system.     

An experimentally controlled extreme drought in a Norway spruce forest reveals fast hydraulic response and subsequent recovery of growth rates

Key message

An experimental drought treatment, exacerbated by a natural drought event, compromised growth in Norway spruce, but more cavitation-resistant xylem was produced and no long-term growth reductions were observed.

Abstract

An experimental drought treatment in a mature Norway spruce forest that coincided with a rare drought event in southern Sweden in 1992, allowed us to study how such forests may respond to similar extreme events in the future. Immediately after the onset of the drought treatment, height and diameter growth decreased compared to control treatments. New xylem cells had smaller lumen und thicker walls, resulting in a more safety-orientated water transport system. The maximum growth and hydraulic system response of the 1990–1996 drought treatment coincided with the 1992 summer drought event. After the drought treatment ended, all measured traits recovered to control and irrigation treatment values after 3 years. While height and diameter growth recovered with delay, wood structure and hydraulic properties showed fast recovery. We conclude that a highly plastic response of the hydraulic system indicates a notable degree of resilience to droughts that are expected to become more common under climate change. Our results do not imply, however, that survival and productivity of Norway spruce plantations would not be compromised under drier conditions in the future, and they apply to site conditions equivalent to the studied system.