The total path length hydraulic resistance according to known anatomical patterns: What is the shape of the root-to-leaf tension gradient along the plant longitudinal axis?

Xylem conduit diameter widens from leaf tip to stem base and how this widening affects the total hydraulic resistance (RTOT) and the gradient of water potential (Ψxyl) has never been thoroughly investigated. Data of conduit diameter of Acer pseudoplatanus,Fagus sylvatica and Picea abies were used to model the axial variation of RTOT and Ψxyl. The majority of RTOT (from 79 to 98%) was predicted to be confined within the leaf/needle. This means that the xylem conduits of stem and roots, accounting for nearly the total length of the hydraulic path, theoretically provide a nearly negligible contribution to RTOT. Consequently, a steep gradient of water potentials was predicted to develop within the leaf/needle base, whereas lower in the stem water potentials approximate those of rootlets. Our results would suggest that the strong partitioning of RTOT between leaves/needles coupled with basal conduit widening is of key importance for both hydraulic safety against drought-induced embolism formation and efficiency, as it minimizes the exposure of stem xylem to high tensions and makes the total plant's conductance substantially independent of body size.

Scots pine trees react to drought by increasing xylem and phloem conductivities.

Drought limits the long-distance transport of water in the xylem due to the reduced leaf-to-soil water potential difference and possible embolism-related losses of conductance and of sugars in the phloem due to the higher viscosity of the dehydrated sugary solution. This condition can have cascading effects in water and carbon (C) fluxes that may ultimately cause tree death. We hypothesize that the maintenance of xylem and phloem conductances is fundamental for survival also under reduced resource availability, when trees may produce effective and low C cost anatomical adjustments in the xylem and phloem close to the treetop where most of the hydraulic resistance is concentrated. We analyzed the treetop xylem and phloem anatomical characteristics in coexisting Scots pine trees, symptomatic and non-symptomatic of drought-induced dieback. We selected the topmost 55 cm of the main stem and selected several sampling positions at different distances from the stem apex to test for differences in the axial patterns between the two groups of trees. We measured the annual ring area, the tracheid hydraulic diameter (Dh) and cell wall thickness (CWT), the conductive phloem area and the average lumen diameter of the 20 largest phloem sieve cells (Dph). Declining trees grew less than the non-declining ones, and despite the similar axial scaling of anatomical traits, had larger Dh and lower CWT. Moreover, declining trees had wider Dph. Our results demonstrate that even under drought stress, maintenance of xylem and phloem efficiencies is of primary importance for survival, even if producing fewer larger tracheids may lead to a xylem more vulnerable to embolism formation.

Vulnerability to xylem embolism correlates to wood parenchyma fraction in angiosperms but not in gymnosperms.

Understanding which structural and functional traits are linked to species' vulnerability to embolism formation (P50) may provide fundamental knowledge on plant strategies to maintain an efficient water transport. We measured P50, wood density (WD), mean conduit area, conduit density, percentage areas occupied by vessels, parenchyma cells (PATOT) and fibers (FA) on branches of angiosperm and gymnosperm species. Moreover, we compiled a dataset of published hydraulic and anatomical data to be compared with our results. Species more vulnerable to embolism had lower WD. In angiosperms, the variability in WD was better explained by PATOT and FA, which were highly correlated. Angiosperms with a higher P50 (less negative) had a higher amount of PATOT and total amount of nonstructural carbohydrates. Instead, in gymnosperms, P50 vs PATOT was not significant. The correlation between PATOT and P50 might have a biological meaning and also suggests that the causality of the commonly observed relationship of WD vs P50 is indirect and dependent on the parenchyma fraction. Our study suggests that angiosperms have a potential active embolism reversal capacity in which parenchyma has an important role, while in gymnosperms this might not be the case.

Hydraulic recovery from xylem embolism in excised branches of twelve woody species: Relationships with parenchyma cells and non-structural carbohydrates.

Embolism repair ability has been documented in numerous species. Although the actual mechanism driving this phenomenon is still debated, experimental findings suggest that non-structural carbohydrates (NSC) stored in wood parenchyma would provide the osmotic forces to drive the refilling of embolized conduits. We selected 12 broadleaved species differing in vulnerability to xylem embolism (P50) and amount of wood parenchyma in order to check direct evidence about the possible link(s) between parenchyma cells abundance, NSC availability and species-specific capacity to reverse xylem embolism. Branches were dehydrated until ∼50% loss of hydraulic conductivity was recorded (PLC ∼50%). Hydraulic recovery (ΔPLC) and NSC content was, then, assessed after 1h of rehydration. Species showed a different ability to recover their hydraulic conductivity from PLC∼50%. Removing the bark in the species showing hydraulic recovery inhibited the embolism reversal. Strong correlations between the ΔPLC and: a) the amount of parenchyma cells (mainly driven by the pith area), b) the consumption of soluble NSC have been recorded. Our results support the hypothesis that refilling of embolized vessels is mediated by the mobilization of soluble NSC and it is mainly recorded in species with a higher percentage of parenchyma cells that may be important in the hydraulic recovery mechanism as a source of carbohydrates and/or as a source of water.

Similarities and differences in the balances between leaf, xylem and phloem structures in Fraxinus ornus along an environmental gradient.

The plant carbon balance depends on the coordination between photosynthesis and the long-distance transport of water and sugars. How plants modify the allocation to the different structures affecting this coordination under different environmental conditions has been poorly investigated. In this study, we evaluated the effect of soil water availability on the allocation to leaf, xylem and phloem structures in Fraxinus ornus L. We selected small individuals of F. ornus (height ~2 m) from sites contrasting in soil water availability (wet vs dry). We measured how the leaf (LM) and stem + branch biomass (SBM) are cumulated along the stem. Moreover, we assessed the axial variation in xylem (XA) and phloem tissue area (PA), and in lumen area of xylem vessels (CAxy) and phloem sieve elements (CAph). We found a higher ratio of LM:SBM in the trees growing under drier conditions. The long-distance transport tissues of xylem and phloem followed axial patterns with scaling exponents (b) independent of site conditions. PA scaled isometrically with XA (b ~ 1). While CAxy was only marginally higher at the wet sites, CAph was significantly higher at the drier sites. Our results showed that under reduced soil water availability, F. ornus trees allocate relatively more to the leaf biomass and produce more conductive phloem, which is likely to compensate for the drought-related hydraulic limitations to the leaf gas exchanges and the phloem sap viscosity.

Tree differences in primary and secondary growth drive convergent scaling in leaf area to sapwood area across Europe.

Trees scale leaf (AL ) and xylem (AX ) areas to couple leaf transpiration and carbon gain with xylem water transport. Some species are known to acclimate in AL  : AX balance in response to climate conditions, but whether trees of different species acclimate in AL  : AX in similar ways over their entire (continental) distributions is unknown. We analyzed the species and climate effects on the scaling of AL vs AX in branches of conifers (Pinus sylvestris, Picea abies) and broadleaved (Betula pendula, Populus tremula) sampled across a continental wide transect in Europe. Along the branch axis, AL and AX change in equal proportion (isometric scaling: b Ëœ 1) as for trees. Branches of similar length converged in the scaling of AL vs AX with an exponent of b = 0.58 across European climates irrespective of species. Branches of slow-growing trees from Northern and Southern regions preferentially allocated into new leaf rather than xylem area, with older xylem rings contributing to maintaining total xylem conductivity. In conclusion, trees in contrasting climates adjust their functional balance between water transport and leaf transpiration by maintaining biomass allocation to leaves, and adjusting their growth rate and xylem production to maintain xylem conductance.

Osmolality and Non-Structural Carbohydrate Composition in the Secondary Phloem of Trees across a Latitudinal Gradient in Europe.

Phloem osmolality and its components are involved in basic cell metabolism, cell growth, and in various physiological processes including the ability of living cells to withstand drought and frost. Osmolality and sugar composition responses to environmental stresses have been extensively studied for leaves, but less for the secondary phloem of plant stems and branches. Leaf osmotic concentration and the share of pinitol and raffinose among soluble sugars increase with increasing drought or cold stress, and osmotic concentration is adjusted with osmoregulation. We hypothesize that similar responses occur in the secondary phloem of branches. We collected living bark samples from branches of adult Pinus sylvestris, Picea abies, Betula pendula and Populus tremula trees across Europe, from boreal Northern Finland to Mediterranean Portugal. In all studied species, the observed variation in phloem osmolality was mainly driven by variation in phloem water content, while tissue solute content was rather constant across regions. Osmoregulation, in which osmolality is controlled by variable tissue solute content, was stronger for Betula and Populus in comparison to the evergreen conifers. Osmolality was lowest in mid-latitude region, and from there increased by 37% toward northern Europe and 38% toward southern Europe due to low phloem water content in these regions. The ratio of raffinose to all soluble sugars was negligible at mid-latitudes and increased toward north and south, reflecting its role in cold and drought tolerance. For pinitol, another sugar known for contributing to stress tolerance, no such latitudinal pattern was observed. The proportion of sucrose was remarkably low and that of hexoses (i.e., glucose and fructose) high at mid-latitudes. The ratio of starch to all non-structural carbohydrates increased toward the northern latitudes in agreement with the build-up of osmotically inactive C reservoir that can be converted into soluble sugars during winter acclimation in these cold regions. Present results for the secondary phloem of trees suggest that adjustment with tissue water content plays an important role in osmolality dynamics. Furthermore, trees acclimated to dry and cold climate showed high phloem osmolality and raffinose proportion.