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      Beyond the extreme: recovery of carbon and water relations in woody plants following heat and drought stress

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          Abstract

          Plant responses to drought and heat stress have been extensively studied, whereas post-stress recovery, which is fundamental to understanding stress resilience, has received much less attention. Here, we present a conceptual stress-recovery framework with respect to hydraulic and metabolic functioning in woody plants. We further synthesize results from controlled experimental studies following heat or drought events and highlight underlying mechanisms that drive post-stress recovery. We find that the pace of recovery differs among physiological processes. Leaf water potential and abscisic acid concentration typically recover within few days upon rewetting, while leaf gas exchange-related variables lag behind. Under increased drought severity as indicated by a loss in xylem hydraulic conductance, the time for stomatal conductance recovery increases markedly. Following heat stress release, a similar delay in leaf gas exchange recovery has been observed, but the reasons are most likely a slow reversal of photosynthetic impairment and other temperature-related leaf damages, which typically manifest at temperatures above 40 °C. Based thereon, we suggest that recovery of gas exchange is fast following mild stress, while recovery is slow and reliant on the efficiency of repair and regrowth when stress results in functional impairment and damage to critical plant processes. We further propose that increasing stress severity, particular after critical stress levels have been reached, increases the carbon cost involved in reestablishing functionality. This concept can guide future experimental research and provides a base for modeling post-stress recovery of carbon and water relations in trees.

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          Most cited references87

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          Vulnerability of Xylem to Cavitation and Embolism

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            A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

            Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.
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              Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited.

              J Flexas (2002)
              There is a long-standing controversy as to whether drought limits photosynthetic CO2 assimilation through stomatal closure or by metabolic impairment in C3 plants. Comparing results from different studies is difficult due to interspecific differences in the response of photosynthesis to leaf water potential and/or relative water content (RWC), the most commonly used parameters to assess the severity of drought. Therefore, we have used stomatal conductance (g) as a basis for comparison of metabolic processes in different studies. The logic is that, as there is a strong link between g and photosynthesis (perhaps co-regulation between them), so different relationships between RWC or water potential and photosynthetic rate and changes in metabolism in different species and studies may be 'normalized' by relating them to g. Re-analysing data from the literature using light-saturated g as a parameter indicative of water deficits in plants shows that there is good correspondence between the onset of drought-induced inhibition of different photosynthetic sub-processes and g. Contents of ribulose bisphosphate (RuBP) and adenosine triphosphate (ATP) decrease early in drought development, at still relatively high g (higher than 150 mmol H20 m(-2) s(-1)). This suggests that RuBP regeneration and ATP synthesis are impaired. Decreased photochemistry and Rubisco activity typically occur at lower g (<100 mmol H20 m(-2) s(-1)), whereas permanent photoinhibition is only occasional, occurring at very low g (<50 mmol H20 m(-2) s(-1)). Sub-stomatal CO2 concentration decreases as g becomes smaller, but increases again at small g. The analysis suggests that stomatal closure is the earliest response to drought and the dominant limitation to photosynthesis at mild to moderate drought. However, in parallel, progressive down-regulation or inhibition of metabolic processes leads to decreased RuBP content, which becomes the dominant limitation at severe drought, and thereby inhibits photosynthetic CO2 assimilation.
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                Author and article information

                Journal
                Tree Physiol
                Tree Physiol
                treephys
                Tree Physiology
                Oxford University Press
                0829-318X
                1758-4469
                August 2019
                17 May 2019
                17 May 2019
                : 39
                : 8
                : 1285-1299
                Affiliations
                [1 ]Karlsruhe Institute of Technology, Institute of Meteorology and Climate Research—Atmospheric Environmental Research (KIT/IMK-IFU), Garmisch-Partenkirchen, Germany
                [2 ]Department of Botany, University of Innsbruck, Innsbruck, Austria
                Author notes
                Corresponding author ( nadine.ruehr@ 123456kit.edu )
                Author information
                http://orcid.org/0000-0001-5989-7463
                Article
                tpz032
                10.1093/treephys/tpz032
                6703153
                30924906
                4c3cd22d-242f-412e-aa5c-17b6eca7fe5c
                © The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 23 August 2018
                : 8 January 2019
                : 13 March 2019
                Page count
                Pages: 15
                Funding
                Funded by: German Federal Ministry of Education and Research
                Funded by: German Research Foundation 10.13039/501100001659
                Award ID: RU-1657/2-1
                Categories
                Review

                carbon allocation,hydraulic conductance,non-structural carbohydrates,post-drought,post-heat,recovery,stress legacy,trees,xylem embolism

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