Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are nonredundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at less negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. This study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.
Xylem cavitation resistance is a key physiological trait correlated with species tolerance to extreme drought stresses. Little is known about the genetic variability and phenotypic plasticity of this trait in natural tree populations. Here we measured the cavitation resistance of 17 Fagus sylvatica populations representative of the full range of the species in Europe. The trees were grown in three field trials under contrasting climatic conditions. Our findings suggest that the genotypic variability of cavitation resistance is high between genotypes of a given population. By contrast, no significant differences were found for this trait across populations, the mean population cavitation resistance being remarkably constant in each trial. We found a significant site effect and a significant site × population interaction, suggesting that cavitation resistance has a high phenotypic plasticity and that this plasticity is under genetic control. The implications of our findings for beech forest management in a context of climate change are discussed.
From 2011 to 2013, Texas experienced its worst drought in recorded history. This event provided a unique natural experiment to assess species-specific responses to extreme drought and mortality of four co-occurring woody species: Quercus fusiformis, Diospyros texana, Prosopis glandulosa, and Juniperus ashei. We examined hypothesized mechanisms that could promote these species' diverse mortality patterns using postdrought measurements on surviving trees coupled to retrospective process modelling. The species exhibited a wide range of gas exchange responses, hydraulic strategies, and mortality rates. Multiple proposed indices of mortality mechanisms were inconsistent with the observed mortality patterns across species, including measures of the degree of iso/anisohydry, photosynthesis, carbohydrate depletion, and hydraulic safety margins. Large losses of spring and summer whole-tree conductance (driven by belowground losses of conductance) and shallower rooting depths were associated with species that exhibited greater mortality. Based on this retrospective analysis, we suggest that species more vulnerable to drought were more likely to have succumbed to hydraulic failure belowground.
Xylem vulnerability to cavitation is a key parameter in understanding drought resistance of trees. We determined the xylem water pressure causing 50% loss of hydraulic conductivity (P(50)), a proxy of vulnerability to cavitation, and we evaluated the variability of this trait at tree and population levels for Fagus sylvatica. We checked for the effects of light on vulnerability to cavitation of stem segments together with a time series variation of P(50). Full sunlight-exposed stem segments were less vulnerable to cavitation than shade-exposed ones. We found no clear seasonal change of P(50), suggesting that this trait was designed for a restricted period. P(50) varied for populations settled along a latitudinal gradient, but not for those sampled along an altitudinal gradient. Moreover, mountainside exposure seemed to play a major role in the vulnerability to cavitation of beech populations, as we observed the differences along north-facing sides but not on south-facing sides. Unexpectedly, both north-facing mountainside and northern populations appeared less vulnerable than those grown on the southern mountainside or in the South of France. These results on beech populations were discussed with respect to the results at within-tree level.
Key message In case of a prolonged drought, the stored carbohydrates in trees were remobilized to fuel survival functions until their nearly depletion at death stage. Abstract Dynamic global vegetation models project forest tree mortality in response to the recurrent severe droughts likely in the future. However, these models should better take into account the physiological processes involved in tree mortality. Faced with severe drought, the Fagus sylvatica L. tree strongly limits its cambial growth. This suggests that readjustments in carbon (C) allocation among sink functions are taking place in response to the lack of water and this could allow tree's survival. For 3 years, we induced a water shortage on 8-year-old beech trees in a rain exclusion system. During this period, we analysed the consequences of severe drought on survival rate, growth, and non-structural carbohydrate (NSC) dynamics in the aboveground and belowground compartments of control, water-stressed living, and dead trees. The survival rate after 3 years of drought was 87%, while primary and secondary growth was strongly reduced. The first 2 years, NSC concentrations increased in all tree compartments (stem, branches, and roots) in response to drought. However, during the third year, starch dropped markedly in water-stressed trees, while soluble sugar concentrations remained similar to control trees. All the compartments in dead trees were virtually empty of starch and soluble sugars. Maintaining an active C storage function at the expense of growth was certainly key to F. sylvatica survival under prolonged extreme drought conditions. Processbased models predicting mortality should better take into account C storage and remobilization processes in forest trees.
The influence of aquaporin (AQP) activity on plant water movement remains unclear, especially in plants subject to unfavorable conditions. We applied a multitiered approach at a range of plant scales to (i) characterize the resistances controlling water transport under drought, flooding and flooding plus salinity conditions; (ii) quantify the respective effects of AQP activity and xylem structure on root (Kroot), stem (Kstem) and leaf (Kleaf) conductances, and (iii) evaluate the impact of AQP-regulated transport capacity on gas exchange. We found that drought, flooding and flooding-salinity reduced Kroot and root AQP activity in Pinus taeda, whereas Kroot of the flood-tolerant Taxodium distichum did not decline under flooding. The extent of the AQP-control of transport efficiency varied among organs and species, ranging from 35%-55% in Kroot to 10%-30% in Kstem and Kleaf. In response to treatments, AQP-mediated inhibition of Kroot rather than changes in xylem acclimation controlled the fluctuations in Kroot. The reduction in stomatal conductance and its sensitivity to vapor pressure deficit were direct responses to decreased whole-plant conductance triggered by lower Kroot and larger resistance belowground. Our results provide new mechanistic and functional insights on plant hydraulics that are essential to quantifying the influences of future stress on ecosystem function.
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