The quandary of sources and sinks of CO2 efflux in tree stems-new insights and future directions.

Stem respiration (RS) substantially contributes to the return of photo assimilated carbon to the atmosphere and, thus, to the tree and ecosystem carbon balance. Stem CO2 efflux (ECO2) is often used as a proxy for RS. However, this metric has often been challenged because of the uncertain origin of CO2 emitted from the stem due to post-respiratory processes. In this Insight, we (i) describe processes affecting the quantification of RS, (ii) review common methodological approaches to quantify and model RS and (iii) develop a research agenda to fill the most relevant knowledge gaps that we identified. Dissolution, transport and accumulation of respired CO2 away from its production site, reassimilation of respired CO2 via stem photosynthesis and the enzyme phosphoenolpyruvate carboxylase, axial CO2 diffusion in the gas phase, shifts in the respiratory substrate and non-respiratory oxygen (O2) consumption are the most relevant processes causing divergence between RS and measured stem gas exchange (ECO2 or O2 influx, IO2). Two common methodological approaches to estimate RS, namely the CO2 mass balance approach and the O2 consumption technique, circumvent some of these processes but have yielded inconsistent results regarding the fate of respired CO2. Stem respiration modelling has recently progressed at the organ and tree levels. However, its implementation in large-scale models, commonly operated from a source-driven perspective, is unlikely to reflect adequate mechanisms. Finally, we propose hypotheses and approaches to advance the knowledge of the stem carbon balance, the role of sap pH on RS, the reassimilation of respired CO2, RS upscaling procedures, large-scale RS modelling and shifts in respiratory metabolism during environmental stress.

More than just CO2 -recycling: corticular photosynthesis as a mechanism to reduce the risk of an energy crisis induced by low oxygen.

Reassimilation of internal CO2 via corticular photosynthesis (PScort ) has an important effect on the carbon economy of trees. However, little is known about its role as a source of O2 supply to the stem parenchyma and its implications in consumption and movement of O2 within trees. PScort of young Populus nigra (black poplar) trees was investigated by combining optical micro-optode measurements with monitoring of stem chlorophyll fluorescence. During times of zero sap flow in spring, stem oxygen concentrations (cO2 ) exhibited large temporal changes. In the sapwood, over 80% of diurnal changes in cO2 could be explained by respiration rates (Rd(mod) ). In the cortex, photosynthetic oxygen release during the day altered this relationship. With daytime illumination, oxygen levels in the cortex steadily increased from subambient and even exhibited a diel period of superoxia of up to 110% (% air sat.). By contrast, in the sapwood, cO2 never reached ambient levels; the diurnal oxygen deficit was up to 25% of air saturation. Our results confirm that PScort is not only a CO2 -recycling mechanism, it is also a mechanism to actively raise the cortical O2 concentration and counteract temporal/spatial hypoxia inside plant stems.

Respiratory adaptations to a combination of oxygen deprivation and extreme carbon dioxide concentration in nematodes.

To examine physiological adaptations to the two combined stressors O2 deprivation and extreme CO2 concentrations, we compared respiratory responses of two nematode species occurring in natural CO2 springs. The minimum O2 concentration allowing maintenance of respiration in both species was 0.0176µmol O2ml-1 (corresponds to 1.4% O2 in air). After exposure to anoxia, individuals resumed respiration immediately when O2 was added, but on a lower level compared to control and without showing a respiratory overshoot. A species-specific response was found in respiration rate during 20% CO2: the more tolerant species maintained respiration rates, whereas the sensitive species showed a decreased respiration rate as low as after anoxia. The results indicate that during 20% CO2 the sensitive species undergo a survival state. We conclude, that the ability to maintain respiration even under low oxygen and high CO2 concentrations may allow the better adapted species to occupy an ecological niche in the field, where others cannot exist.

Bark and woody tissue photosynthesis: a means to avoid hypoxia or anoxia in developing stem tissues.

In woody plants, oxygen transport and delivery via the xylem sap are well described, but the contribution of bark and woody tissue photosynthesis to oxygen delivery in stems is poorly understood. Here, we combined stem chlorophyll fluorescence measurements with microsensor quantifications of bark O2 levels and oxygen gas exchange measurements of isolated current-year stem tissues of beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) to investigate how bark and woody tissue photosynthesis impairs the oxygen status of stems. Measurements were made before bud break, when the axial path of oxygen supply via the xylem sap is impeded. At that time, bark O2 levels showed O2 concentrations below the atmospheric concentration, indicating hypoxic conditions or O2 deficiency within the inner bark, but the values were always far away from anoxic. Under illumination bark and woody tissue photosynthesis rapidly increased internal oxygen concentrations compared with plants in the dark, and thereby counteracted against localised hypoxia. The highest photosynthetic activity and oxygen release rates were found in the outermost cortex tissues. By contrast, rates of woody tissue photosynthesis were considerably lower, due to the high light attenuation of the bark and cortex tissues, as well as resistances in radial oxygen diffusion. Therefore, our results confirm that bark and woody tissue photosynthesis not only play a role in plant carbon economy, but may also be important for preventing low oxygen-limitations of respiration in these dense and metabolically active tissues.

General trait relationships in stems: a study on the performance and interrelationships of several functional and structural parameters involved in corticular photosynthesis.

We addressed corticular photosynthesis, focusing on parameters of underlying dark and light reactions as well as structural differentiation. To unveil general stem traits and underlying principles that may be valid across several tree species, CO(2) exchange rates and chlorophyll-fluorescence parameters were measured in current-year to 3-year-old stems of five deciduous tree species (including climax and pioneer species). Across species, dark CO(2) efflux rates (R(d)) of stems exhibited a common regression relationship with photosynthetic rates (A) and light-adapted quantum efficiency of photosystem II (PSII) (Delta F/Fm'), a pattern analogous to leaf trait correlations. Furthermore, A and Delta F/Fm' were closely interrelated to each other. Consistent correlations of stem structure and function were also assessed among species. Changes in tissue structure during ageing significantly affected several stem functional parameters. Stem CO(2) efflux during the dark and corticular photosynthetic rates declined with increasing stem age as well as light-adapted quantum efficiency of PSII. Furthermore, a strong relationship between stem R(d) and peridermal PFD-transmittance (T) as well as between R(d) and total bark chlorophyll was evident. Consistent results were found for the relationships between corticular photosynthesis (or primary photosynthetic reactions like Delta F/Fm') and selected structural traits. The found correlation patterns among functional and/or structural traits of stems and their concordance with leaf trait relationships may aid in identifying underlying mechanisms and scaling relationships that link traits to plant and ecosystem function.

Effects of ozone impact on the gas exchange and chlorophyll fluorescence of juvenile birch stems (Betula pendula Roth.).

Effects of ozone impact on gas exchange and chlorophyll fluorescence of juvenile birch (Betula pendula) stems and leaves were investigated. Significant differences in the response of leaves and stems to ozone were found. In leaves, O3 exposure led to a significant decline in photosynthetic rates, whereas stems revealed an increased dark respiration and a concomitant increase in corticular photosynthesis. In contrast to birch leaves, corticular photosynthesis appeared to support the carbon balance of stems or even of the whole-tree under O3 stress. The differences in the ozone-response between leaves and stems were found to be related to ozone uptake rates, and thus to inherent differences in leaf and stem O3 conductance.

Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees.

Temperature dependencies of stem dark respiration (R(d)) and light-driven bark photosynthesis (A(max)) of two temperate tree species (Fagus sylvatica and Betula pendula) were investigated to estimate their probable influence on stem carbon balance. Stem R(d) was found to increase exponentially with increasing temperatures, whereas A(max) levelled off or decreased at the highest temperatures chosen (35-40 degrees C). Accordingly, a linear relationship between respiratory and assimilatory metabolism was only found at moderate temperatures (10-30 degrees C) and the relationship between stem R(d) and A(max) clearly departed from linearity at chilling (5 degrees C) and at high temperatures (35-40 degrees C). As a result, the proportional internal C-refixation rate also decreased non-linearly with increasing temperature. Temperature response of photosystem II (PSII) photochemistry was also assessed. Bark photochemical yield (Delta F/F(m)') followed the same temperature pattern as bark CO(2) assimilation. Maximum quantum yield of PSII (F(v)/F(m)) decreased drastically at freezing temperatures (-5 degrees C), while from 30 to 40 degrees C only a marginal decrease in F(v)/F(m) was found. In in situ measurements during winter months, bark photosynthesis was found to be strongly reduced. Low temperature stress induced an active down-regulation of PSII efficiency as well as damage to PSII due to photoinhibition. All in all, the benefit of bark photosynthesis was negatively affected by low (<5 degrees C) as well as high temperatures (>30 degrees C). As the carbon balance of tree stems is defined by the difference between photosynthetic carbon gain and respiratory carbon loss, this might have important implications for accurate modelling of stem carbon balance.

Stem CO2 release under illumination: corticular photosynthesis, photorespiration or inhibition of mitochondrial respiration?

In illuminated stems and branches, CO2 release is often reduced. Many light-triggered processes are thought to contribute to this reduction, namely photorespiration, corticular photosynthesis or even an inhibition of mitochondrial respiration. In this study, we investigated these processes with the objective to discriminate their influence to the overall reduction of branch CO2 release in the light. CO2 gas-exchange measurements of young birch (Betula pendula Roth.) branches (< 1.5 cm) performed under photorespiratory (20% O2) and non-photorespiratory (< 2%) conditions revealed that photorespiration does not play a pre-dominant role in carbon exchange. This suppression of photorespiration was attributed to the high CO2 concentrations (C(i)) within the bark tissues (1544 +/- 227 and 618 +/- 43 micromol CO2 mol(-1) in the dark and in the light, respectively). Changes in xylem CO2 were not likely to explain the observed decrease in stem CO2 release as gas-exchange measurements before and after cutting of the branches did not effect CO2 efflux to the atmosphere. Combined fluorescence and gas-exchange measurements provided evidence that the light-dependent reduction in CO2 release can pre-dominantly be attributed to corticular refixation, whereas an inhibition of mitochondrial respiration in the light is unlikely to occur. Corticular photosynthesis was able to refix up to 97% of the CO2 produced by branch respiration, although it rarely led to a positive net photosynthetic rate.