Lidewei Vergeynst

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.

Changes in stem water content influence sap flux density measurements with thermal dissipation probes

Key messageStem WC may decline during the day. Zero-flowdTmincreases when WC decreases. Use of nighttimedTmin the calculation of sap flux density during the day might introduce errors.AbstractThere is increasing evidence of diel variation in water content of stems of living trees as a result of changes in internal water reserves. The interplay between dynamic water storage and sap flow is of current interest, but the accuracy of measurement of both variables has come into question. Fluctuations in stem water content may induce inaccuracy in thermal-based measurements of sap flux density because wood thermal properties are dependent on water content. The most widely used thermal method for measuring sap flux density is the thermal dissipation probe (TDP) with continuous heating, which measures the influence of moving sap on the temperature difference between a heated needle and a reference needle vertically separated in the flow stream. The objective of our study was to investigate how diel fluctuations in water content could influence TDP measurements of sap flux density. We analysed the influence of water content on the zero-flow maximum temperature difference, dTm, which is used as the reference for calculating sap flux density, and present results of a dehydration experiment on cut branch segments of American sycamore (Platanus occidentalis L.). We demonstrate both theoretically and experimentally that dTm increases when stem water content declines. Because dTm is measured at night when water content is high, this phenomenon could result in underestimations of sap flux density during the day when water content is lower. We conclude that diel dynamics in water content should be considered when TDP is used to measure sap flow.Stem WC may decline during the day. Zero-flow dT m increases when WC decreases. Use of nighttime dT m in the calculation of sap flux density during the day might introduce errors. There is increasing evidence of diel variation in water content of stems of living trees as a result of changes in internal water reserves. The interplay between dynamic water storage and sap flow is of current interest, but the accuracy of measurement of both variables has come into question. Fluctuations in stem water content may induce inaccuracy in thermal-based measurements of sap flux density because wood thermal properties are dependent on water content. The most widely used thermal method for measuring sap flux density is the thermal dissipation probe (TDP) with continuous heating, which measures the influence of moving sap on the temperature difference between a heated needle and a reference needle vertically separated in the flow stream. The objective of our study was to investigate how diel fluctuations in water content could influence TDP measurements of sap flux density. We analysed the influence of water content on the zero-flow maximum temperature difference, dT m, which is used as the reference for calculating sap flux density, and present results of a dehydration experiment on cut branch segments of American sycamore (Platanus occidentalis L.). We demonstrate both theoretically and experimentally that dT m increases when stem water content declines. Because dT m is measured at night when water content is high, this phenomenon could result in underestimations of sap flux density during the day when water content is lower. We conclude that diel dynamics in water content should be considered when TDP is used to measure sap flow.

Capacitive water release and internal leaf water relocation delay drought-induced cavitation in African Maesopsis eminii

The impact of drought on the hydraulic functioning of important African tree species, like Maesopsis eminii Engl., is poorly understood. To map the hydraulic response to drought-induced cavitation, sole reliance on the water potential at which 50% loss of xylem hydraulic conductivity (ψ50) occurs might be limiting and at times misleading as the value alone does not give a comprehensive overview of strategies evoked by M. eminii to cope with drought. This article therefore uses a methodological framework to study the different aspects of drought-induced cavitation and water relations in M. eminii. Hydraulic functioning of whole-branch segments was investigated during bench-top dehydration. Cumulative acoustic emissions and continuous weight measurements were used to quantify M. eminiis vulnerability to drought-induced cavitation and hydraulic capacitance. Wood structural traits, including wood density, vessel area, diameter and wall thickness, vessel grouping index, solitary vessel index and vessel wall reinforcement, were used to underpin observed physiological responses. On average, M. eminiis ψ50 (±SE) was -1.9 ± 0.1 MPa, portraying its xylem as drought vulnerable, just as one would expect for a common tropical pioneer. However, M. eminii additionally employed an interesting desiccation delay strategy, fuelled by internal relocation of leaf water, hydraulic capacitance and the presence of parenchyma around the xylem vessels. Our findings suggest that exclusive dependence on ψ50 would have misdirected our assessments of M. eminiis drought stress vulnerability. Hydraulic capacitance linked to anatomy and leaf-water relocation behaviour was equally important to better understand M. eminiis drought survival strategies. Because our study was conducted on branches of 3-year-old greenhouse-grown M. eminii seedlings, the findings cannot be simply extrapolated to adult M. eminii trees or their mature wood, because structural and physiological plant properties change with age. The techniques and methodological framework used in this study are, however, transferable to other species regardless of age.

Deciphering acoustic emission signals in drought stressed branches: the missing link between source and sensor

When drought occurs in plants, acoustic emission (AE) signals can be detected, but the actual causes of these signals are still unknown. By analyzing the waveforms of the measured signals, it should, however, be possible to trace the characteristics of the AE source and get information about the underlying physiological processes. A problem encountered during this analysis is that the waveform changes significantly from source to sensor and lack of knowledge on wave propagation impedes research progress made in this field. We used finite element modeling and the well-known pencil lead break source to investigate wave propagation in a branch. A cylindrical rod of polyvinyl chloride was first used to identify the theoretical propagation modes. Two wave propagation modes could be distinguished and we used the finite element model to interpret their behavior in terms of source position for both the PVC rod and a wooden rod. Both wave propagation modes were also identified in drying-induced signals from woody branches, and we used the obtained insights to provide recommendations for further AE research in plant science.