Imperforate tracheary elements and vessels alleviate xylem tension under severe dehydration: insights from water release curves for excised twigs of three tree species

Abstract

Premise Water stored in the xylem of woody plants is important for supporting the transpiration stream under prolonged drought, yet the source of stored water within the xylem during drought remains unclear. Insights into xylem water utilization during drought will uncover the adaptation strategies of the test species to stress. Methods To fill the existing knowledge gap, we excised twigs of Abies firma (Japanese fir, conifer), Cercidiphyllum japonicum (katsura tree, diffuse‐porous) and Quercus serrata (konara oak, ring‐porous) to quantify interspecific variation of water transfer in xylem corresponding with increasing cumulative water release (CWR) using micro x‐ray computed tomography and cryo‐SEM. Results For all species studied, the main components of water storage within the operating range of water potential were not living cells but cavitation release and capillaries. Abies firma maintained water in the earlywood‐like cells, for possible maintenance of the transpiration stream. Cercidiphyllum japonicum maintained water in its vessels over 200 kg m‐3 of CWR, while Q. serrata lost most of its water in vessels with increasing CWR up to 100 kg m‐3. Cercidiphyllum japonicum exhibited a higher water storage capacity than Q. serrata. Under high CWR, narrow conduits stored xylem water in C. japonicum and imperforate tracheary elements in Q. serrata. Conclusions Among the species examined, increasing CWR appears to indicate differential utilization of stored water in relation to variation of xylem structure, thereby providing insight into the interspecific responses of tree species to drought.

Functional xylem characteristics associated with drought‐induced embolism in angiosperms

“…In addition to the uncertainty concerning de novo drought‐induced embolism, it remains largely unknown what happens to xylem sap that is released when vessels become fully embolised. It is possible that the water displaced by the formation of water vapour may be released into the transpiration stream or taken up by cell walls or cytoplasm of living xylem cells (Vergeynst et al ., 2015; Yazaki et al ., 2020). At the same time, the process of embolisation itself may temporarily reduce the chances of air seeding in adjacent vessels, based on a modelling study that suggests that gas may be extracted from adjacent tissues via interconduit pit membranes during the initial stages of embolisation (Wang et al ., 2015).…”

“…connectivity, vessel widening) and their interaction on whole‐plant transpiration, construction costs and carbon income. Furthermore, accurate 3D models should include tissue capacitance (Gleason et al ., 2014; Yazaki et al ., 2020), which would clear the way towards evaluating the consequences of water storage in the short term (subsecond, seconds) and long term (minutes, hours, days). Finally, an integrative whole‐plant model should be parameterised and validated with experimental results from methods that allow studying changes in the liquid and gas phase in xylem sap at a high temporal resolution (Pereira et al ., 2020; Jansen et al ., 2022), and should also account for variation in hydraulic demand during developmental plant stages across multiple species from different plant functional groups.…”

Size-related changes in leaf, wood, and bark traits in even-aged <i>Falcataria falcata</i> trees

“…The increase in both WWC and WD in the outer xylem of larger trees would reflect the increased fractions of vessel lumens, which are key water storage places (Yazaki et al 2020;Zieminska et al 2020) and thickening of fiber-cell walls, respectively, as found in Indonesia (Ishiguri et al 2009). The increase in vessel fractions and probably in vessel diameter along the size would be important to mitigate the size-related increase in hydraulic resistance (e.g., Olson et al 2014;Azuma et al 2022).…”

Plasticity in branch water relations and stem hydraulic vulnerability enhances hydraulic safety in mangroves growing along a salinity gradient

“…In contrast, no positive correlations were found between stem C TLP and anatomy in A. corniculatum , raising the possibility that water discharged from storage may be sourced broadly from both living tissues and apoplastic spaces. Indeed, studies have suggested that water released from the apoplast in xylem tissues through cavitation of fibres and vessels may also act as a capacitor (Baer et al, 2021; Cai et al, 2014; Gessler, 2021; Knipfer et al, 2019; Yazaki et al, 2020; Zweifel et al, 2014), with spatial variation in cavitation enhancing the maintenance of hydration required for survival of critical living tissues during extreme drought conditions (Barigah et al, 2013). Further research is required to understand the patterns of water loss and retention within stems of intact plants in relation to their function under increasing water stress induced by drought and salinity.…”