Jasper Bloemen

Transport of root‐respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees

Upward transport of CO₂ via the transpiration stream from belowground to aboveground tissues occurs in tree stems. Despite potentially important implications for our understanding of plant physiology, the fate of internally transported CO₂ derived from autotrophic respiratory processes remains unclear. We infused a ¹³CO₂-labeled aqueous solution into the base of 7-yr-old field-grown eastern cottonwood (Populus deltoides) trees to investigate the effect of xylem-transported CO₂ derived from the root system on aboveground carbon assimilation and CO₂ efflux. The ¹³C label was transported internally and detected throughout the tree. Up to 17% of the infused label was assimilated, while the remainder diffused to the atmosphere via stem and branch efflux. The largest amount of assimilated ¹³C was found in branch woody tissues, while only a small quantity was assimilated in the foliage. Petioles were more highly enriched in ¹³C than other leaf tissues. Our results confirm a recycling pathway for respired CO₂ and indicate that internal transport of CO₂ from the root system may confound the interpretation of efflux-based estimates of woody tissue respiration and patterns of carbohydrate allocation.

Woody tissue photosynthesis in trees: salve on the wounds of drought?

Drought-induced tree stress has gained increasing interest because of the recent coupling between forest decline and global change associated droughts (Allen et al., 2010; Anderegg et al., 2012, 2013; Martinez-Vilalta et al., 2012; McDowell et al., 2013b; Zeppel et al., 2013; IPCC, 2014; Doughty et al., 2015; Hartmann et al., 2015). To synthesize existing knowledge on drought stress and mortality mechanisms, McDowell et al. (2008) proposed the widely applied hydraulic failure and carbon starvation hypotheses. Hydraulic failure manifests when plants irreversibly desiccate due to uncontrolled air intrusion in the water transport system. Air intrusion, or cavitation, has dual consequences: at moderate level it may improve plant water status by local tension release and water supply to the transpiration stream (Vergeynst et al., 2015), but progressive cavitation and excessive conductivity loss will ultimately lead to mortality (Tyree & Sperry, 1988). Trees may minimize the risk of hydraulic failure by closing their stomata, but this also limits CO2 uptake. Prolonged stomatal closure may eventually lead to a negative plant carbon balance and ultimately carbon starvation (Zhao et al., 2013). A distinction has been made between anisohydric tree species that operate at narrow hydraulic safety margins and are more susceptible to hydraulic failure, and isohydric tree species that prevent lethal cavitation by tightly regulating stomatal conductance, which makes them more susceptible to carbon starvation (McDowell et al., 2008). For both functional tree types, pests and biotic agents such as insects or pathogens may either weaken the trees before droughtinduced tree mortality or accelerate the actual mortality process (Gaylord et al., 2013; Oliva et al., 2014). While providing a good framework, the hydraulic failure and carbon starvation hypotheses have been the focus of intense debate and further research. Tree mortality experiments indicate that a much more complex reality exists, in which hydraulic and carbon dynamics are strongly interlinked (Adams et al., 2009; McDowell, 2011; Sala et al., 2012; McDowell et al., 2013a,b; Mitchell et al., 2013; O’Grady et al., 2013; Sevanto, 2014; Sevanto et al., 2014; Hartmann et al., 2015). Recent studies indicate that isohydric and anisohydric tree species show both hydraulic failure and carbon starvation characteristics, evoking the image of a drought response continuum rather than a strict distinction between isohydricity and anisohydricity (Mitchell et al., 2013; Sevanto et al., 2014). Furthermore, it has been suggested that more isohydric species have the lowest hydraulic safety margins and the highest capacity to repair xylem cavitation (Meinzer & McCulloh, 2013). These examples indicate the high complexity of intertwined mechanisms supporting tree life under drought, and, when failing, leading to death. As indicated by Zeppel et al. (2011) and Martinez-Vilalta et al. (2012), the research field of tree mortality is, even though rapidly progressing, still in its infancy. While drought has been shown to rapidly affect the plant water balance adversely (Hartmann et al., 2013), carbon processes must not be neglected in mortality studies as water and carbon processes are closely linked (McDowell, 2011; Steppe et al., 2015). Besides the possible limitation of CO2 uptake due to stomatal closure, drought may induce hydraulic constraints on the transport of nonstructural carbon (NSC) between the different plant compartments, inducing local carbon deficits (Ruehr et al., 2009; Sala et al., 2010; Sevanto, 2014). However, even with local presence of carbohydrates, other drought-induced processes might deplete these local pools to maintain the hydraulic integrity and negate the effects of xylem cavitation, such as osmoregulation (Sevanto et al., 2014), embolism refilling (Secchi&Zwieniecki, 2012) and sensing (Zwieniecki & Holbrook, 2009). These carbohydrates are then unavailable for regularmetabolicmaintenance processes, leading to carbon starvation (McDowell & Sevanto, 2010). Hence, carbon starvation is not just a question of the carbon storage pool size, but primarily of the local availability of carbon for cell survival in sink tissues. Surprisingly, woody tissue photosynthesis as a means of providing carbon locally by recycling respired CO2 via photosynthesis in chlorophyll containing woody tissues (stem recycling photosynthesis; Avila et al., 2014) has received little to no attention throughout the mortality discussion.

Stem girdling affects the quantity of CO2 transported in xylem as well as CO2 efflux from soil

There is recent clear evidence that an important fraction of root-respired CO2 is transported upward in the transpiration stream in tree stems rather than fluxing to the soil. In this study, we aimed to quantify the contribution of root-respired CO2 to both soil CO2 efflux and xylem CO2 transport by manipulating the autotrophic component of belowground respiration. We compared soil CO2 efflux and the flux of root-respired CO2 transported in the transpiration stream in girdled and nongirdled 9-yr-old oak trees (Quercus robur) to assess the impact of a change in the autotrophic component of belowground respiration on both CO2 fluxes. Stem girdling decreased xylem CO2 concentration, indicating that belowground respiration contributes to the aboveground transport of internal CO2 . Girdling also decreased soil CO2 efflux. These results confirmed that root respiration contributes to xylem CO2 transport and that failure to account for this flux results in inaccurate estimates of belowground respiration when efflux-based methods are used. This research adds to the growing body of evidence that efflux-based measurements of belowground respiration underestimate autotrophic contributions.

Assimilation of xylem-transported CO2 is dependent on transpiration rate but is small relative to atmospheric fixation

The effect of transpiration rate on internal assimilation of CO2 released from respiring cells has not previously been quantified. In this study, detached branches of Populus deltoides were allowed to take up (13)CO2-labelled solution at either high (high label, HL) or low (low label, LL) (13)CO2 concentrations. The uptake of the (13)CO2 label served as a proxy for the internal transport of respired CO2, whilst the transpiration rate was manipulated at the leaf level by altering the vapour pressure deficit (VPD) of the air. Simultaneously, leaf gas exchange was measured, allowing comparison of internal CO2 assimilation with that assimilated from the atmosphere. Subsequent (13)C analysis of branch and leaf tissues revealed that woody tissues assimilated more label under high VPD, corresponding to higher transpiration, than under low VPD. More (13)C was assimilated in leaf tissue than in woody tissue under the HL treatment, whereas more (13)C was assimilated in woody tissue than in leaf tissue under the LL treatment. The ratio of (13)CO2 assimilated from the internal source to CO2 assimilated from the atmosphere was highest for the branches under the HL and high VPD treatment, but was relatively small regardless of VPD×label treatment combination (up to 1.9%). These results showed that assimilation of internal CO2 is highly dependent on the rate of transpiration and xylem sap [CO2]. Therefore, it can be expected that the relative contribution of internal CO2 recycling to tree carbon gain is strongly dependent on factors controlling transpiration, respiration, and photosynthesis.

Internal Recycling of Respired CO 2 May Be Important for Plant Functioning under Changing Climate Regimes

Recent studies have provided evidence of a large flux of root-respired CO2 in the transpiration stream of trees. In our study, we investigated the potential impact of this internal CO2 transport on aboveground carbon assimilation and CO2 efflux. To trace the transport of root-respired CO2, we infused a 13C label at the stem base of field-grown Populus deltoides Bartr. ex. Marsh trees. The 13C label was transported to the top of the stem and throughout the crown via the transpiration stream. Up to 17% of the 13C label was assimilated by chlorophyll-containing tissues. Our results provide evidence of a mechanism for recycling respired CO2 within trees. Such a mechanism may have important implications for how plants cope with predicted increases in intensity and frequency of droughts. Here, we speculate on the potential significance of this recycling mechanism within the context of plant responses to climate change and plants currently inhabiting arid environments.

Root xylem CO2 flux: an important but unaccounted-for component of root respiration

Key messageIn tree roots, a large fractionof root-respired CO2remains within the root system rather than diffusing into the soil. This CO2is transported in xylem sap into the shoot, and because respiration is almost always measured as the flux of CO2into the atmosphere from plant tissues, it represents an unaccounted-for component of tree root metabolism.AbstractRoot respiration has been considered a large component of forest soil CO2 efflux, but recent findings indicate that it may be even more important than previous measurements have shown because a substantial fraction of root-respired CO2 remains within the tree root system and moves internally with the transpiration stream. The high concentration of CO2 in roots appears to originate mainly within the root. It has been suggested that plants can take up dissolved inorganic carbon (DIC) from soil, but under most conditions uptake from soil is minimal due to the root-to-soil diffusion gradient, which suggests that most of the CO2 in root xylem is derived from root respiration. Estimates of the internal flux of CO2 through root xylem are based on combined measurements of sap flow and internal [CO2]. Results quantifying root xylem CO2 flux, obtained for a limited number of species, have raised important concerns regarding our understanding of tree respiration. Taken together, the results of these studies call into question the partitioning of ecosystem respiration into its above- and belowground components, and redefine the energetic costs of tree root metabolism and hence estimates of belowground carbon allocation. Expanding our observations of root xylem CO2 flux to more species and at longer time scales, as well as improving the techniques used to study this process, could be fruitful avenues for future research, with the potential to substantially revise our understanding of root respiration and forest carbon cycles.

Emissions of biogenic volatile organic compounds from Fraxinus excelsior and Quercus robur under ambient conditions in Flanders (Belgium)

A dynamic branch enclosure system was used to measure emission rates of biogenic volatile organic compounds (BVOCs) from two common European tree species: Fraxinus excelsior and Quercus robur under ambient conditions in Flanders (Belgium). Both tree species were studied for seasonal variability of BVOC emission rates under natural biotic stress (infestations). Emissions were normalized at standard conditions of temperature and photosynthetic active radiation (PAR) (30°C and 1000 µmol m−2 s−1, respectively). Emission rates from Fraxinus excelsior were highest in May (9.56 µg gDW −1 h−1) and lowest in October (1.17 µg gDW −1 h−1). This tree species emitted (Z)-β-ocimene, (E)-β-ocimene and α-farnesene during the entire measurement period and additionally isoprene only in May. Quercus robur showed isoprene emission variations according to the seasonal cycle with rates of 30, 106 and 29 µg gDW −1 h−1 in May, August and October, respectively. Apart from isoprene, (E)-β-ocimene and β-caryophyllene were emitted through the entire experimental period.