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      Interaction of stomatal behaviour and vulnerability to xylem cavitation determines the drought response of three temperate tree species

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          Abstract

          How the mortality and growth of tree species vary with the iso-anisohydric continuum and xylem vulnerability is still being debated. We conducted a precipitation reduction experiment to create a mild drought condition in a forest in the Baotianman Mountains, China, a sub-humid region. Three main sub-canopy tree species in this region were examined. After rainfall reduction, Lindera obtusiloba showed severe dieback, but two other co-occurring species did not show dieback. The water potential at stomatal closure of Dendrobenthamia japonica, L. obtusiloba and Sorbus alnifolia was −1.70, −2.54 and −3.41 MPa, respectively, whereas the water potential at 88 % loss in hydraulic conductivity of the three species was −2.31, −2.11 and −7.01 MPa, respectively. Taken together, near-anisohydric L. obtusiloba with vulnerable xylem was highly susceptible to drought dieback. Anisohydric S. alnifolia had the most negative minimum water potential, and its xylem was the most resistant to cavitation. Isohydric D. japonica conserved water by rapidly closing its stomata. Ultimately, the hydraulic safety margin (HSM) of L. obtusiloba was the smallest among the three species, especially in precipitation-reduced plots. In terms of the stomatal safety margin (SSM), L. obtusiloba was negative, while S. alnifolia and D. japonica were positive. Of the two species without dieback, rainfall reduction decreased growth of D. japonica, but did not influence growth of S. Alnifolia; meanwhile, rainfall reduction led to a decrease of non-structural carbohydrates (NSCs) in D. japonica, but an increase in S. alnifolia. It is concluded that HSM as well as SSM allow interpreting the sensitivity of the three sub-canopy species to drought. The drought-induced dieback of L. obtusiloba is determined by the interaction of stomatal behaviour and xylem vulnerability, and the species could be sensitive to climate change-caused drought although still in sub-humid areas. The isohydric/anisohydric degree is associated with NSCs status and growth of plants.

          Abstract

          Climate change-induced drought has caused increasing plant mortality around the globe. In this study, we artificially reduced annual rainfall in the field of temperate continental mountains, and investigated different responses of three understory tree species to drought and their response strategies. This study aimed to explore how future climate change-caused droughts might affect vegetation succession in the region. Plants have two important attributes that regulate water balance: closable pores in leaves (stomata) and long-distance water transport channels (xylem conduits). It was found that the synergistic effect of stomatal adjustment and xylem anti-embolism ability was the key to drought resistance.

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          Most cited references28

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          Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality.

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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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              A method for measuring hydraulic conductivity and embolism in xylem

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                Author and article information

                Contributors
                Role: Editor
                Journal
                AoB Plants
                AoB Plants
                aobpla
                AoB Plants
                Oxford University Press (US )
                2041-2851
                October 2019
                23 September 2019
                23 September 2019
                : 11
                : 5
                : plz058
                Affiliations
                [1 ] Institute of New Forestry Technology, Chinese Academy of Forestry , Beijing, China
                [2 ] Key Laboratory of Forest Ecology and Environment of State Forestry Administration, Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry , Beijing, China
                Author notes
                Corresponding author’s e-mail address: wxc@ 123456caf.ac.cn
                Article
                plz058
                10.1093/aobpla/plz058
                6802943
                c38ff864-d330-436e-90ac-88058fcb9057
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 10 January 2019
                : 19 August 2019
                : 04 September 2019
                : 21 October 2019
                Page count
                Pages: 14
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31290223
                Award ID: 31800513
                Award ID: 31270648
                Funded by: Institute of New Forestry Technology
                Funded by: Chinese Academy of Forestry 10.13039/501100005197
                Award ID: CAFYBB2017SY047
                Categories
                Studies

                Plant science & Botany
                anisohydric,carbon starvation,climate change,hydraulic failure,isohydric,xylem vulnerability

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