Shifting access to pools of shoot water sustains gas exchange and increases stem hydraulic safety during seasonal atmospheric drought.

acclimation capacitance drought tolerance dry season hydraulic safety margins leaf mangrove pressure-volume curves shoot stem

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
09 2021
Historique:
revised: 30 04 2021
received: 04 11 2020
accepted: 01 05 2021
pubmed: 12 5 2021
medline: 15 12 2021
entrez: 11 5 2021
Statut: ppublish

Résumé

Understanding how plants acclimate to drought is crucial for predicting future vulnerability, yet seasonal acclimation of traits that improve drought tolerance in trees remains poorly resolved. We hypothesized that dry season acclimation of leaf and stem traits influencing shoot water storage and hydraulic capacitance would mitigate the drought-associated risks of reduced gas exchange and hydraulic failure in the mangrove Sonneratia alba. By late dry season, availability of stored water had shifted within leaves and between leaves and stems. While whole shoot capacitance remained stable, the symplastic fraction of leaf water increased 86%, leaf capacitance increased 104% and stem capacitance declined 80%. Despite declining plant water potentials, leaf and whole plant hydraulic conductance remained unchanged, and midday assimilation rates increased. Further, the available leaf water between the minimum water potential observed and that corresponding to 50% loss of stem conductance increased 111%. Shifting availability of pools of water, within and between organs, maintained leaf water available to buffer periods of increased photosynthesis and losses in stem hydraulic conductivity, mitigating risks of carbon depletion and hydraulic failure during atmospheric drought. Seasonal changes in access to tissue and organ water may have an important role in drought acclimation and avoidance.

Identifiants

pubmed: 33974303
doi: 10.1111/pce.14080
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2898-2911

Informations de copyright

© 2021 John Wiley & Sons Ltd.

Références

Abrams, M. D., & Kubiske, M. E. (1990). Photosynthesis and water relations during drought in Acer rubrum L. genotypes from contrasting sites in Central Pennsylvania. Functional Ecology, 4, 727-733.
Adams, H. D., Zeppel, M. J. B., Anderegg, W. R. L., Hartmann, H., Landhäusser, S. M., Tissue, D. T., … McDowell, N. G. (2017). A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nature Ecology & Evolution, 1, 1285-1291.
Allen, C. D., & Breshears, D. D. (2007). Climate-induced forest dieback as an emergent global phenomenon. Eos, Transactions American Geophysical Union, 88, 504-504.
Allen, C. D., Breshears, D. D., & McDowell, N. G. (2015). On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere, 6, 1-55.
Anderegg, W. R. L., Klein, T., Bartlett, M., Sack, L., Pellegrini, A. F. A., Choat, B., & Jansen, S. (2016). Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America, 113, 5024-5029.
Ball, M. C., & Pidsley, S. M. (1995). Growth responses to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata, in northern Australia. Functional Ecology, 9, 77-85.
Bartlett, M. K., Detto, M., & Pacala, S. W. (2019). Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade-offs among plant hydraulic traits. Ecology Letters, 22, 67-77.
Bartlett, M. K., Klein, T., Jansen, S., Choat, B., & Sack, L. (2016). The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proceedings of the National Academy of Sciences of the United States of America, 113, 13098-13103.
Bartlett, M. K., Scoffoni, C., & Sack, L. (2012). The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: A global meta-analysis. Ecology Letters, 15, 393-405.
Bartlett, M. K., Zhang, Y., Kreidler, N., Sun, S., Ardy, R., Cao, K., & Sack, L. (2014). Global analysis of plasticity in turgor loss point, a key drought tolerance trait. Ecology Letters, 17, 1580-1590.
Beedlow, P. A., Waschmann, R. S., Lee, E. H., & Tingey, D. T. (2017). Seasonal patterns of bole water content in old growth Douglas-fir (Pseudotsuga menziesii [Mirb.] Franco). Agricultural and Forest Meteorology, 242, 109-119.
Binks, O., Meir, P., Rowland, L., da Costa, A. C. L., Vasconcelos, S. S., de Oliveira, A. A. R., … Mencuccini, M. (2016). Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytologist, 211, 477-488.
Blackman, C. J., Pfautsch, S., Choat, B., Delzon, S., Gleason, S. M., & Duursma, R. A. (2016). Toward an index of desiccation time to tree mortality under drought. Plant, Cell & Environment, 39, 2342-2345.
Brodribb, T. J., & Holbrook, N. M. (2003). Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology, 132, 2166-2173.
Brodribb, T. J., Holbrook, N. M., Edwards, E. J., & Gutiérrez, M. V. (2003). Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell & Environment, 26, 443-450.
Brodribb, T. J., Powers, J., Cochard, H., & Choat, B. (2020). Hanging by a thread? Forests and drought. Science, 368, 261-266.
Bryant C. (2019). Foliar surface water uptake and hydraulic function in the mangrove, Sonneratia alba (Honours thesis). Australian National University.
Bucci, S. J., Goldstein, G., Scholz, F. G., & Meinzer, F. C. (2016). Physiological significance of hydraulic segmentation, nocturnal transpiration and capacitance in tropical trees: Paradigms revisited. In G. Goldstein & L. S. Santiago (Eds.), Tropical tree physiology: Adaptations and responses in a changing environment (pp. 205-225). Cham: Springer International Publishing.
Carrasco, L. O., Bucci, S. J., Di Francescantonio, D., Lezcano, O. A., Campanello, P. I., Scholz, F. G., … Goldstein, G. (2015). Water storage dynamics in the main stem of subtropical tree species differing in wood density, growth rate and life history traits. Tree Physiology, 35, 354-365.
Chimenti, C. A., & Hall, A. J. (1994). Responses to water stress of apoplastic water fraction and bulk modulus of elasticity in sunflower (Helianthus annuus L.) genotypes of contrasting capacity for osmotic adjustment. Plant and Soil, 166, 101-107.
Choat, B., Jansen, S., Brodribb, T. J., Cochard, H., Delzon, S., Bhaskar, R., … Zanne, A. E. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752-755.
Chou, C., Chiang, J. C. H., Lan, C.-W., Chung, C.-H., Liao, Y.-C., & Lee, C.-J. (2013). Increase in the range between wet and dry season precipitation. Nature Geoscience, 6, 263-267.
Davy, R., Esau, I., Chernokulsky, A., Outten, S., & Zilitinkevich, S. (2017). Diurnal asymmetry to the observed global warming. International Journal of Climatology, 37, 79-93.
de Cárcer, P. S., Vitasse, Y., Peñuelas, J., Jassey, V. E. J., Buttler, A., & Signarbieux, C. (2018). Vapor-pressure deficit and extreme climatic variables limit tree growth. Global Change Biology, 24, 1108-1122.
Duke, N., Ball, M., & Ellison, J. (1998). Factors influencing biodiversity and distributional gradients in mangroves. Global Ecology & Biogeography Letters, 7, 27-47.
Duursma, R. A., Blackman, C. J., Lopéz, R., Martin-StPaul, N. K., Cochard, H., & Medlyn, B. E. (2019). On the minimum leaf conductance: Its role in models of plant water use, and ecological and environmental controls. New Phytologist, 221, 693-705.
Eamus, D., Boulain, N., Cleverly, J., & Breshears, D. D. (2013). Global change-type drought-induced tree mortality: Vapor pressure deficit is more important than temperature per se in causing decline in tree health. Ecology and Evolution, 3, 2711-2729.
Epila, J., De Baerdemaeker, N. J. F., Vergeynst, L. L., Maes, W. H., Beeckman, H., & Steppe, K. (2017). Capacitive water release and internal leaf water relocation delay drought-induced cavitation in African Maesopsis eminii. Tree Physiology, 37, 481-490.
Epron, D., & Dreyer, E. (1993). Long-term effects of drought on photosynthesis of adult oak trees [Quercus petraea (Matt.) Liebl. and Quercus robur L.] in a natural stand. New Phytologist, 125, 381-389.
Ewers, F. W. & Fisher, J. B. (1989). Techniques for measuring vessel lengths and diameters in stems of woody plants. American Journal of Botany, 76, 645-656.
Ficklin, D. L., & Novick, K. A. (2017). Historic and projected changes in vapor pressure deficit suggest a continental-scale drying of the United States atmosphere. Journal of Geophysical Research: Atmospheres, 122, 2061-2079.
Flexas, J., Bota, J., Escalona, J. M., Sampol, B., & Medrano, H. (2002). Effects of drought on photosynthesis in grapevines under field conditions: An evaluation of stomatal and mesophyll limitations. Functional Plant Biology, 29, 461-471.
Gleason, S. M., Blackman, C. J., Cook, A. M., Laws, C. A., & Westoby, M. (2014). Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats. Tree Physiology, 34, 275-284.
Grossiord, C., Buckley, T. N., Cernusak, L. A., Novick, K. A., Poulter, B., Siegwolf, R. T. W., … McDowell, N. G. (2020). Plant responses to rising vapor pressure deficit. New Phytologist, 226, 1550-1566.
Hao, G.-Y., Sack, L., Wang, A.-Y., Cao, K.-F., & Goldstein, G. (2010). Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Functional Ecology, 24, 731-740.
Hao, G.-Y., Wheeler, J. K., Holbrook, N. M., & Goldstein, G. (2013). Investigating xylem embolism formation, refilling and water storage in tree trunks using frequency domain reflectometry. Journal of Experimental Botany, 64, 2321-2332.
Harvey, H. W. (1966). The chemistry and fertility of sea waters. Cambridge: Cambridge University Press.
Hochberg, U., Albuquerque, C., Rachmilevitch, S., Cochard, H., David-Schwartz, R., Brodersen, C. R., … Windt, C. W. (2016). Grapevine petioles are more sensitive to drought induced embolism than stems: Evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation. Plant, Cell & Environment, 39, 1886-1894.
Hsiao, T. C. (1973). Plant responses to water stress. Ann Rev. Plant Physiology, 24, 519-570.
John, G. P., Henry, C., & Sack, L. (2018). Leaf rehydration capacity: Associations with other indices of drought tolerance and environment. Plant, Cell & Environment, 41, 2638-2653.
Joly, R. J., & Zaerr, J. B. (1987). Alteration of cell-wall water content and elasticity in Douglas-Fir during periods of water deficit. Plant Physiology, 83, 418-422.
Kerstiens, G. (1996). Cuticular water permeability and its physiological significance. Journal of Experimental Botany, 47, 1813-1832.
Körner, C. (2019). No need for pipes when the well is dry-A comment on hydraulic failure in trees. Tree Physiology, 39, 695-700.
Kozlowski, T. T., & Pallardy, S. G. (1997). Physiology of woody plants (2nd ed.). San Diego, CA: Academic Press.
Kozlowski, T. T., & Pallardy, S. G. (2002). Acclimation and adaptive responses of woody plants to environmental stresses. The Botanical Review, 68, 270-334.
Kursar, T. A., Engelbrecht, B. M. J., Burke, A., Tyree, M. T., Omari, B. E., & Giraldo, J. P. (2009). Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution. Functional Ecology, 23, 93-102.
Larcher, W. (2003). Physiological plant ecology: Ecophysiology and stress physiology of functional groups. Berlin, Heidelberg: Springer Science & Business Media.
Li, X., Delzon, S., Torres-Ruiz, J., Badel, E., Burlett, R., Cochard, H., … Choat, B. (2020). Lack of vulnerability segmentation in four angiosperm tree species: Evidence from direct X-ray microtomography observation. Annals of Forest Science, 77, 37.
Mantova, M., Menezes-Silva, P. E., Badel, E., Cochard, H., & Torres-Ruiz, J. M. (2021). The interplay of hydraulic failure and cell vitality explains tree capacity to recover from drought. Physiologia Plantarum, 172, 247-257.
Martinez-Vilalta, J., Anderegg, W. R. L., Sapes, G., & Sala, A. (2019). Greater focus on water pools may improve our ability to understand and anticipate drought-induced mortality in plants. New Phytologist, 223, 22-32.
Matheny, A. M., Bohrer, G., Garrity, S. R., Morin, T. H., Howard, C. J., & Vogel, C. S. (2015). Observations of stem water storage in trees of opposing hydraulic strategies. Ecosphere, 6, art165.
Maury, P., Berger, M., Mojayad, F., & Planchon, C. (2000). Leaf water characteristics and drought acclimation in sunflower genotypes. Plant and Soil, 223, 155-162.
McCulloh, K. A., Johnson, D. M., Meinzer, F. C., & Woodruff, D. R. (2014). The dynamic pipeline: Hydraulic capacitance and xylem hydraulic safety in four tall conifer species. Plant, Cell & Environment, 37, 1171-1183.
Meehl, G. A., & Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science, 305, 994-997.
Meinzer, F. C., Johnson, D. M., Lachenbruch, B., McCulloh, K. A., & Woodruff, D. R. (2009). Xylem hydraulic safety margins in woody plants: Coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology, 23, 922-930.
Melcher, P. J., Meinzer, F. C., Yount, D. E., Goldstein, G., & Zimmermann, U. (1998). Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe. Journal of Experimental Botany, 49, 1757-1760.
Nguyen, H. T., Meir, P., Sack, L., Evans, J. R., Oliveira, R. S., & Ball, M. C. (2017). Leaf water storage increases with salinity and aridity in the mangrove Avicennia marina: Integration of leaf structure, osmotic adjustment and access to multiple water sources. Plant, Cell & Environment, 40, 1576-1591.
Ogburn, R. M., & Edwards, E. J. (2010). Chapter 4 - the ecological water-use strategies of succulent plants. In J.-C. Kader & M. Delseny (Eds.), Advances in Botanical Research (pp. 179-225). Cambridge, Massachusetts: Academic Press.
Ogle, K., Barber, J. J., Willson, C., & Thompson, B. (2009). Hierarchical statistical modeling of xylem vulnerability to cavitation. New Phytologist, 182, 541-554.
Pearcy, R., Schulze, E. & Zimmermann, R. (2000). Measurement of transpiration and leaf conductance. In Pearcy, R. Ehlering, J., Mooney, H., & Rundel, P (Eds.), Plant physiological ecology (pp. 137-160). Dordrecht: Springer.
Pereira, L., Bittencourt, P. R. L., Oliveira, R. S., Junior, M. B. M., Barros, F. V., Ribeiro, R. V., & Mazzafera, P. (2016). Plant pneumatics: Stem air flow is related to embolism - New perspectives on methods in plant hydraulics. New Phytologist, 211, 357-370.
Pivovaroff, A. L., Sack, L., & Santiago, L. S. (2014). Coordination of stem and leaf hydraulic conductance in southern California shrubs: A test of the hydraulic segmentation hypothesis. New Phytologist, 203, 842-850.
Rodriguez-Dominguez, C. M., Murphy, M. R. C., Lucani, C., & Brodribb, T. J. (2018). Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytologist, 218, 1025-1035.
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
Rosas, T., Mencuccini, M., Barba, J., Cochard, H., Saura-Mas, S., & Martínez-Vilalta, J. (2019). Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytologist, 223, 632-646.
Sack, L., Cowan, P. D., Jaikumar, N., & Holbrook, N. M. (2003). The ‘hydrology’ of leaves: Co-ordination of structure and function in temperate woody species. Plant, Cell & Environment, 26, 1343-1356.
Sack, L., Medeiros, C. D., Scoffoni, C., John, G. P., Bartlett, M. K., Inman-Narahari, F., … Price, J. (2018). Using a broad suite of traits, including hydraulics, for robust prediction of species and forest vital rates in space and time. AGU Fall Meeting Abstracts, 2018, B11B-B2146B.
Saliendra, N. Z., & Meinzer, F. C. (1991). Symplast volume, turgor, stomatal conductance and growth in relation to osmotic and elastic adjustment in droughted sugarcane. Journal of Experimental Botany, 42, 1251-1259.
Salomón, R. L., Steppe, K., Ourcival, J. M., Villers, S., Rodríguez-Calcerrada, J., Schapman, R., & Limousin, J. M. (2020). Hydraulic acclimation in a Mediterranean oak subjected to permanent throughfall exclusion results in increased stem hydraulic capacitance. Plant, Cell & Environment, 43, 1528-1544.
Sanders, G. J., & Arndt, S. K. (2012). Osmotic adjustment under drought conditions. In R. Aroca (Ed.), Plant responses to drought stress. Berlin, Heidelberg: Springer.
Sapes, G., Roskilly, B., Dobrowski, S., Maneta, M., Anderegg, W. R. L., Martinez-Vilalta, J., & Sala, A. (2019). Plant water content integrates hydraulics and carbon depletion to predict drought-induced seedling mortality. Tree Physiology, 39, 1300-1312.
Scholz, F. G., Phillips, N. G., Bucci, S. J., Meinzer, F. C., & Goldstein, G. (2011). Hydraulic capacitance: Biophysics and functional significance of internal water sources in relation to tree size. In F. C. Meinzer, B. Lachenbruch, & T. E. Dawson (Eds.), Size- and age-related changes in tree structure and function (pp. 341-361). Dordrecht, the Netherlands: Springer Netherlands.
Skelton, R. P., Brodribb, T. J., & Choat, B. (2017). Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytologist, 214, 561-569.
Trenberth, K. E., Dai, A., van der Schrier, G., Jones, P. D., Barichivich, J., Briffa, K. R., & Sheffield, J. (2014). Global warming and changes in drought. Nature Climate Change, 4, 17-22.
Tsuda, M., & Tyree, M. T. (1997). Whole-plant hydraulic resistance and vulnerability segmentation in Acer saccharinum. Tree Physiology, 17, 351-357.
Tyree, M. T., Cochard, H., Cruiziat, P., Sinclair, B., & Ameglio, T. (1993). Drought-induced leaf shedding in walnut: Evidence for vulnerability segmentation. Plant, Cell & Environment, 16, 879-882.
Tyree, M. T., Engelbrecht, B. M. J., Vargas, G., & Kursar, T. A. (2003). Desiccation tolerance of five tropical seedlings in Panama. Relationship to a field assessment of drought performance. Plant Physiology, 132, 1439-1447.
Tyree, M. T., & Hammel, H. T. (1972). The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany, 23, 267-282.
Vendramini, F., Díaz, S., Gurvich, D. E., Wilson, P. J., Thompson, K., & Hodgson, J. G. (2002). Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytologist, 154, 147-157.
Vilagrosa, A., Morales, F., Abadía, A., Bellot, J., Cochard, H., & Gil-Pelegrin, E. (2010). Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species. Environmental and Experimental Botany, 69, 233-242.
Wolf, A., Anderegg, W. R. L., & Pacala, S. W. (2016). Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proceedings of the National Academy of Sciences of the United States of America, 113, E7222-E7230.
Yuan, W., Zheng, Y., Piao, S., Ciais, P., Lombardozzi, D., Wang, Y., … Yang, S. (2019). Increased atmospheric vapor pressure deficit reduces global vegetation growth. Science Advances, 5, eaax1396.
Zhang, Y., Lamarque, L. J., Torres-Ruiz, J. M., Schuldt, B., Karimi, Z., Li, S., … Jansen, S. (2018). Testing the plant pneumatic method to estimate xylem embolism resistance in stems of temperate trees. Tree Physiology, 38, 1016-1025.
Zimmerman, M. (1983). Xylem structure and the ascent of sap. Berlin: Springer Science & Business Media.

Auteurs

Callum Bryant (C)

Plant Science Division, Research School of Biology, Australian National University, Acton, Australia.

Tomas I Fuenzalida (TI)

Plant Science Division, Research School of Biology, Australian National University, Acton, Australia.

Nigel Brothers (N)

Plant Science Division, Research School of Biology, Australian National University, Acton, Australia.

Maurizio Mencuccini (M)

Catalan Institution for Research and Advanced Studies, Barcelona, Spain.
Ecological and Forestry Applications Research Centre, Barcelona, Spain.

Lawren Sack (L)

Department of Ecology and Evolution, University of California Los Angeles, Los Angeles, California, USA.

Oliver Binks (O)

Plant Science Division, Research School of Biology, Australian National University, Acton, Australia.

Marilyn C Ball (MC)

Plant Science Division, Research School of Biology, Australian National University, Acton, Australia.

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