Teemu Hölttä

Assimilate transport in phloem sets conditions for leaf gas exchange

Carbon uptake and transpiration in plant leaves occurs through stomata that open and close. Stomatal action is usually considered a response to environmental driving factors. Here we show that leaf gas exchange is more strongly related to whole tree level transport of assimilates than previously thought, and that transport of assimilates is a restriction of stomatal opening comparable with hydraulic limitation. Assimilate transport in the phloem requires that osmotic pressure at phloem loading sites in leaves exceeds the drop in hydrostatic pressure that is due to transpiration. Assimilate transport thus competes with transpiration for water. Excess sugar loading, however, may block the assimilate transport because of viscosity build-up in phloem sap. Therefore, for given conditions, there is a stomatal opening that maximizes phloem transport if we assume that sugar loading is proportional to photosynthetic rate. Here we show that such opening produces the observed behaviour of leaf gas exchange. Our approach connects stomatal regulation directly with sink activity, plant structure and soil water availability as they all influence assimilate transport. It produces similar behaviour as the optimal stomatal control approach, but does not require determination of marginal cost of water parameter.

Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation.

Measurements of diurnal diameter variations of the xylem and phloem are a promising tool for studying plant hydraulics and xylem-phloem interactions in field conditions. However, both the theoretical framework and the experimental verification needed to interpret phloem diameter data are incomplete. In this study, we analytically evaluate the effects of changing the radial conductance between the xylem and the phloem on phloem diameter variations and test the theory using simple manipulation experiments. Our results show that phloem diameter variations are mainly caused by changes in the radial flow rate of water between the xylem and the phloem. Reducing the hydraulic conductance between these tissues decreases the amplitude of phloem diameter variation and increases the time lag between xylem and phloem diameter variation in a predictable manner. Variation in the amplitude and timing of diameter variations that cannot be explained by changes in the hydraulic conductance, could be related to changes in the osmotic concentration in the phloem.

Capacitive effect of cavitation in xylem conduits: results from a dynamic model

Embolisms decrease plant hydraulic conductance and therefore reduce the ability of the xylem to transport water to leaves provided that embolized conduits are not refilled. However, as a xylem conduit is filled with gas during cavitation, water is freed to the transpiration stream and this transiently increases xylem water potential. This capacitive effect of embolism formation on plant function has not been explicitly quantified in the past. A dynamic model is presented that models xylem water potential, xylem sap flow and cavitation, taking into account both the decreasing hydraulic conductance and the water release effect of xylem embolism. The significance of the capacitive effect increases in relation to the decreasing hydraulic conductance effect when transpiration rate is low in relation to the total amount of water in xylem conduits. This ratio is typically large in large trees and during drought.

The effect of artificially induced drought on radial increment and wood properties of Norway spruce

We studied experimentally the effects of water availability on height and radial increment as well as wood density and tracheid properties of Norway spruce (Picea abies (L.) Karst.). The study was carried out in two long-term N-fertilization experiments in Southern Finland (Heinola and Sahalahti). At each site, one fertilized and one control plot was covered with an under-canopy roof preventing rainwater from reaching the soil. Two uncovered plots were monitored at each site. The drought treatment was initiated in the beginning of growing season and lasted for 60-75 days each year. The treatment was repeated for four to five consecutive years depending on the site. Altogether, 40 sample trees were harvested and discs sampled at breast height. From the discs, ring width and wood density were measured by X-ray densitometry. Tracheid properties were analysed by reflected-light microscopy and image analysis. Reduced soil water potential during the growing season decreased annual radial and height increment and had a small influence on tracheid properties and wood density. No statistically significant differences were found in the average tracheid diameter between the drought-treated and control trees. The average cell wall thickness was somewhat higher (7-10%) for the drought treatment than for the control, but the difference was statistically significant only in Sahalahti. An increased cell wall thickness was found in both early- and latewood tracheids, but the increase was much greater in latewood. In drought-treated trees, cell wall proportion within an annual ring increased, consequently increasing wood density. No interaction between the N fertilization and drought treatment was found in wood density. After the termination of the drought treatment, trees rapidly recovered from the drought stress. According to our results, severe drought due to the predicted climate change may reduce Norway spruce growth but is unlikely to result in large changes in wood properties.

Coordination of physiological traits involved in drought‐induced mortality of woody plants

Accurate modelling of drought-induced mortality is challenging. A steady-state model is presented integrating xylem and phloem transport, leaf-level gas exchange and plant carbohydrate consumption during drought development. A Bayesian analysis of parameter uncertainty based on expert knowledge and a literature review is carried out. The model is tested by combining six data compilations covering 170 species using information on sensitivities of xylem conductivity, stomatal conductance and leaf turgor to water potential. The possible modes of plant failure at steady state are identified (i.e. carbon (C) starvation, hydraulic failure and phloem transport failure). Carbon starvation occurs primarily in the parameter space of isohydric stomatal control, whereas hydraulic failure is prevalent in the space of xylem susceptibility to embolism. Relative to C starvation, phloem transport failure occurs under conditions of low sensitivity of photosynthesis and high sensitivity of growth to plant water status. These three failure modes are possible extremes along two axes of physiological vulnerabilities, one characterized by the balance of water supply and demand and the other by the balance between carbohydrate sources and sinks. Because the expression of physiological vulnerabilities is coordinated, we argue that different failure modes should occur with roughly equal likelihood, consistent with predictions using optimality theory.

Fluxes of carbon dioxide and water vapour over Scots pine forest and clearing

The carbon dioxide and water vapour fluxes were measured by the eddy covariance (EC) technique from July to September 2000 at two closely located sites in southern Finland: over a 38-year-old pine forest and over a 5-year-old forest clearing. The night-time respiration was of the same magnitude at both sites. At day-time the pine forest was a strong sink but the clearing close to CO2 balance, indicating that CO2 uptake of ground vegetation over the clearing balanced the release from the soil. The shoot scale gas exchange measurements in combination with process-based modelling were used to evaluate the measured CO2 exchange of the forest ecosystem. The forest CO2 exchange was explained by soil respiration and photosynthesis of forest canopy, while the contribution of understory and ground vegetation CO2 exchange could be neglected. During the study period the forest was a net sink of CO2 and the clearing a source. The daily average uptake of CO2 by the forest was −2.4 and − 1.7 gm −2 per day in July–August and September periods, respectively; and average release by the clearing 4.0 and 2.5 g m −2 per day during the same periods. This shows that carbon losses 5 years after clear-cutting are substantial. The evapotranspiration (ET) was higher over the forest compared to clearing as a result of transpiration from the forest canopy. The difference in ET was small during the July–August period when precipitation frequently occurred.

Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal

· Currently, phloem transport in plants under field conditions is not well understood. This is largely the result of the lack of techniques suitable for the measurement of the physiological properties of phloem. · We present a model that interprets the changes in xylem diameter and live bark thickness and separates the components responsible for such changes. We test the predictions from this model on data from three mature Scots pine trees in Finland. The model separates the live bark thickness variations caused by bark water capacitance from a residual signal interpreted to indicate the turgor changes in the bark. · The predictions from the model are consistent with processes related to phloem transport. At the diurnal scale, this signal is related to patterns of photosynthetic activity and phloem loading. At the seasonal scale, bark turgor showed rapid changes during two droughts and after two rainfall events, consistent with physiological predictions. Daily cumulative totals of this turgor term were related to daily cumulative totals of canopy photosynthesis. Finally, the model parameter representing radial hydraulic conductance between phloem and xylem showed a temperature dependence consistent with the temperature-driven changes in water viscosity. · We propose that this model has potential for the continuous field monitoring of tree phloem function.

A physiological model of softwood cambial growth

Cambial growth was modelled as a function of detailed levelled physiological processes for cell enlargement and water and sugar transport to the cambium. Cambial growth was described at the cell level where local sugar concentration and turgor pressure induce irreversible cell expansion and cell wall synthesis. It was demonstrated how transpiration and photosynthesis rates, metabolic and physiological processes and structural features of a tree mediate their effects directly on the local water and sugar status and influence cambial growth. Large trees were predicted to be less sensitive to changes in the transient water and sugar status, compared with smaller ones, as they have more water and sugar storage and were, therefore, less coupled to short-term changes in the environment. Modelling the cambial dynamics at the individual cell level turned out to be a complex task as the radial short-distance transport of water and sugars and control signals determining cell division and cessation of cell enlargement and cell wall synthesis had to be described simultaneously.

Comparison of phloem and xylem hydraulic architecture in Picea abies stems

The hydraulic properties of xylem and phloem differ but the magnitude and functional consequences of the differences are not well understood. Phloem and xylem functional areas, hydraulic conduit diameters and conduit frequency along the stems of Picea abies trees were measured and expressed as allometric functions of stem diameter and distance from stem apex. Conductivities of phloem and xylem were estimated from these scaling relations. Compared with xylem, phloem conduits were smaller and occupied a slightly larger fraction of conducting tissue area. Ten times more xylem than phloem was annually produced along the stem. Scaling of the conduit diameters and cross-sectional areas with stem diameter were very similar in phloem and xylem. Phloem and xylem conduits scaled also similarly with distance from stem apex; widening downwards from the tree top, and reaching a plateau near the base of the living crown. Phloem conductivity was estimated to scale similarly to the conductivity of the outermost xylem ring, with the ratio of phloem to xylem conductivity being c. 2%. However, xylem conductivity was estimated to increase more than phloem conductivity with increasing tree dimensions as a result of accumulation of xylem sapwood. Phloem partly compensated for its smaller conducting area and narrower conduits by having a slightly higher conduit frequency.

Separating water-potential induced swelling and shrinking from measured radial stem variations reveals a cambial growth and osmotic concentration signal

The quantification of cambial growth over short time periods has been hampered by problems to discern between growth and the swelling and shrinking of a tree stem. This paper presents a model, which separates cambial growth and reversible water-potential induced diurnal changes from simultaneously measured whole stem and xylem radial variations, from field-measured Scots pine trees in Finland. The modelled growth, which includes osmotic concentration changes, was compared with (direct) dendrometer measurements and microcore samples. In addition, the relationship of modelled growth and dendrometer measurements to environmental factors was analysed. The results showed that the water-potential induced changes of tree radius were successfully separated from stem growth. Daily growth predicted by the model exhibited a high correlation with the modelled daily changes of osmotic concentration in phloem, and a temperature dependency in early summer. Late-summer growth saw higher dependency on water availability and temperature. Evaluation of the model against dendrometer measurements showed that the latter masked a true environmental signal in stem growth due to water-potential induced changes. The model provides better understanding of radial growth physiology and offers potential to examine growth dynamics and changes due to osmotic concentration, and how the environment affects growth.