Identifying the pathways for foliar water uptake in beech (Fagus sylvatica L.): a major role for trichomes.
apoplastic and symplastic
beech (Fagus sylvatica L.)
electron microscopy
fluorescent tracers
foliar absorption
pathways
plant cell walls
silver nanoparticles
synchrotron-based microcomputed tomography
trichomes
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
17
01
2020
revised:
20
03
2020
accepted:
27
03
2020
pubmed:
13
4
2020
medline:
6
3
2021
entrez:
13
4
2020
Statut:
ppublish
Résumé
Foliar water uptake (FWU), the direct uptake of water into leaves, is a global phenomenon, having been observed in an increasing number of plant species. Despite the growing recognition of its functional relevance, our understanding of how FWU occurs and which foliar surface structures are implicated, is limited. In the present study, fluorescent and ionic tracers, as well as microcomputed tomography, were used to assess potential pathways for water entry in leaves of beech, a widely distributed tree species from European temperate regions. Although none of the tracers entered the leaf through the stomatal pores, small amounts of silver precipitation were observed in some epidermal cells, indicating moderate cuticular uptake. Trichomes, however, were shown to absorb and redistribute considerable amounts of ionic and fluorescent tracers. Moreover, microcomputed tomography indicated that 72% of empty trichomes refilled during leaf surface wetting and microscopic investigations revealed that trichomes do not have a cuticle but are covered with a pectin-rich cell wall layer. Taken together, our findings demonstrate that foliar trichomes, which exhibit strong hygroscopic properties as a result of their structural and chemical design, constitute a major FWU pathway in beech.
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
769-780Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Benz, B.W. and Martin, C.E. (2006) Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). J. Plant Physiol. 163, 648-656.
Benzing, D.H. (1976) Bromeliad trichomes: structure, function, and ecological significance. Selbyana, 1, 330-348.
Berry, Z.C., Emery, N.C., Gotsch, S.G. and Goldsmith, G.R. (2019) Foliar water uptake: processes, pathways, and integration into plant water budgets. Plant, Cell Environ. 42, 410-423.
Bickford, C.P. (2016) Ecophysiology of leaf trichomes. Funct. Plant Biol. 43, 807-814.
Boanares, D., Ferreira, B.G., Kozovits, A.R., Sousa, H.C., Isaias, R.M.S. and França, M.G.C. (2018) Pectin and cellulose cell wall composition enables different strategies to leaf water uptake in plants from tropical fog mountain. Plant Physiol. Biochem. 122, 57-64.
Breshears, D.D., McDowell, N.G., Goddard, K.L., Dayem, K.E., Martens, S.N., Meyer, C.W. and Brown, K.M. (2008) Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology, 89, 41-47.
Burgess, S.S.O. and Dawson, T.E. (2004) The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant, Cell Environ. 27, 1023-1034.
Burkhardt, J. (2010) Hygroscopic particles on leaves: Nutrients or desiccants? Ecol. Monogr. 80, 369-399.
Burkhardt, J., Basi, S., Pariyar, S. and Hunsche, M. (2012) Stomatal penetration by aqueous solutions - an update involving leaf surface particles. New Phytol. 196, 774-787.
Dawson, T.E. and Goldsmith, G.R. (2018) The value of wet leaves. New Phytol. 219, 1156-1169.
Dietrich, L. and Kahmen, A. (2019) Water relations of drought-stressed temperate trees benefit from short drought-intermitting rainfall events. Agric. For. Meteorol. 265, 70-77.
Eller, C.B., Lima, A.L. and Oliveira, R.S. (2013) Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytol. 199, 151-162.
Eller, C.B., Lima, A.L. and Oliveira, R.S. (2016) Cloud forest trees with higher foliar water uptake capacity and anisohydric behavior are more vulnerable to drought and climate change. New Phytol. 211, 489-501.
Evert, R.F. (2006) Esau’s Plant Anatomy. Meristems, Cells, and Tissues of the Plant Body: Their Structure, Function, and Development, 3rd edn. Hoboken, NJ: John Wiley and Sons Inc.
Fernández, V., Sancho-Knapik, D., Guzmán, P. et al. (2014) Wettability, polarity, and water absorption of Holm Oak leaves: effect of leaf side and age. Plant Physiol. 166, 168-180.
Fernández, V., Bahamonde, H.A., Peguero-Pina, J.J., Gil-Pelegrín, E., Sancho-Knapik, D., Gil, L., Goldbach, H.E. and Eichert, T. (2017) Physico-chemical properties of plant cuticles and their functional and ecological significance. J. Exp. Bot. 68, 5293-5306.
Gorsuch, J.W. and Klaine, S.J. (1998) Toxicity and fate of silver in the environment. Environ. Toxicol. Chem. 17, 537-538.
Gouvra, E. and Grammatikopoulos, G. (2003) Beneficial effects of direct foliar water uptake on shoot water potential of five chasmophytes. Can. J. Bot. 81, 1278-1284.
Harris, A.T. and Bali, R. (2008) On the formation and extent of uptake of silver nanoparticles by live plants. J. Nanopart. Res. 10, 691-695.
IPCC (2018) Global Warming of 1.5°C. In An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty (Masson-Delmotte, V., Zhai, P., Pörtner, H.-O., Roberts, D., Skea, J., Shukla, P. R., Pirani, A., Moufouma-Okia, W., Péan, C., Pidcock, R., Connors, S., Matthews, J. B. R., Chen, Y., Zhou, X., Gomis, M. I., Lonnoy, E., Maycock, T., Tignor, M. and Waterfield, T. eds). Geneva: IPCC.
Kangur, O., Kupper, P. and Sellin, A. (2017) Predawn disequilibrium between soil and plant water potentials in light of climate trends predicted for northern Europe. Reg. Environ. Change, 17, 2159-2168.
Ketel, D.H., Dirkse, W.G. and Ringoet, A. (1972) Water uptake from foliar-applied drops and its further distribution in the oat leaf. Acta Botanica Neerlandica, 21, 155-166.
Krishnamurthy, K.V. (1999) Methods in Cell Wall Cytochemistry. Boca Raton, FL: CRC Press.
Leroux, O., Eder, M., Saxe, F., Dunlop, J.W.C., Popper, Z.A., Viane, R.L.L. and Knox, J.P. (2018) Comparative in situ analysis reveals the dynamic nature of sclerenchyma cell walls of the fern Asplenium rutifolium. Ann. Bot. 121, 345-358.
Liesche, J., Ziomkiewicz, I. and Schulz, A. (2013) Super-resolution imaging with Pontamine Fast Scarlet 4BS enables direct visualization of cellulose orientation and cell connection architecture in onion epidermis cells. BMC Plant Biol. 13, 226.
Limm, E.B. and Dawson, T.E. (2010) Polystichum munitum (Dryopteridaceae) varies geographically in its capacity to absorb fog water by foliar uptake within the redwood forest ecosystem. Am. J. Bot. 97, 1121-1128.
Limm, E.B., Simonin, K.A., Bothman, A.G. and Dawson, T.E. (2009) Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia, 161, 449-459.
Llamas, F., Perez-Morales, C., Acedo, C. and Penas, A. (1995) Foliar trichomes of the evergreen and semi- deciduous species of the genus Quercus (Fagaceae) in the Iberian Peninsula. Bot. J. Linn. Soc. 117, 47-57.
MacDougall, A.J. and Ring, S.G. (2003) The hydration behaviour of pectin networks and plant cell walls. In Advances in Pectin and Pectinase Research. (Voragen, F., Schols, H. and Visser, R., eds). Dordrecht: Springer, pp. 123-135.
Martin, C.E. and von Willert, D.J. (2000) Leaf epidermal hydathodes and the ecophysiological consequences of foliar water uptake in species of Crassula from the Namib Desert in Southern Africa. Plant Biol. 2, 229-242.
Ohrui, T., Nobira, H., Sakata, Y. et al. (2007) Foliar trichome- and aquaporin-aided water uptake in a drought-resistant epiphyte Tillandsia ionantha Planchon. Planta, 227, 47-56.
Oksanen, E. (2018) Trichomes form an important first line of defence against adverse environment - new evidence for ozone stress mitigation. Plant, Cell Environ. 41, 1497-1499.
Pina, A.L.C.B., Zandavalli, R.B., Oliveira, R.S., Martins, F.R. and Soares, A.A. (2016) Dew absorption by the leaf trichomes of Combretum leprosum in the Brazilian semiarid region. Funct. Plant Biol. 43, 851-861.
Purcell, T.W. and Peters, J.J. (1998) Sources of silver in the environment. Environ. Toxicol. Chem. 17, 539-546.
R Core Team (2018) The R Project for Statistical Computing. Vienna: R Foundation for Statistical Computing.
Ruzin, S.E. (1999) Plant Microtechnique and Microscopy. New York, NY: Oxford University Press.
Schlechter, R.O., Miebach, M. and Remus-Emsermann, M.N.P. (2019) Driving factors of epiphytic bacterial communities: a review. J. Adv. Res. 19, 57-65.
Schmitt, A.K., Martin, C.E. and Lüttge, U.E. (1989) Gas exchange and water vapor uptake in the atmospheric CAM Bromeliad Tillandsia recurvata L.: the influence of trichomes. Botanica Acta, 102, 80-84.
Schönherr, J. (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J. Exp. Bot. 57, 2471-2491.
Schreel, J.D.M. and Steppe, K. (2019) Foliar water uptake changes the world of tree hydraulics. NPJ Clim. Atmos. Sci. 2, 1.
Schreel, J.D.M. and Steppe, K. (2020) Foliar water uptake in trees: negligible or necessary? Trends Plant Sci., in press. https://doi.org/10.1016/j.tplants.2020.01.003
Schreel, J.D.M., von der Crone, J.S., Kangur, O. and Steppe, K. (2019a) Influence of drought on foliar water uptake capacity of temperate tree species. Forests 10, 562.
Schreel, J.D.M., Van de Wal, B.A.E., Hervé-Fernandez, P., Boeckx, P. and Steppe, K. (2019b) Hydraulic redistribution of foliar absorbed water causes turgor-driven growth in mangrove seedlings. Plant, Cell Environ. 42, 2437-2447.
Schreiber, L. and Riederer, M. (1996) Ecophysiology of cuticular transpiration: comparative investigation of cuticular water permeability of plant species from different habitats. Oecologia, 107, 426-432.
Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrasruct Res. 26, 31-43.
Steppe, K., Vandegehuchte, M.W., Van de Wal, B.A.E., Hoste, P., Guyot, A., Lovelock, C.E. and Lockington, D.A. (2018) Direct uptake of canopy rainwater causes turgor-driven growth spurts in the mangrove Avicennia marina. Tree Physiol. 38, 979-991.
Verhertbruggen, Y., Marcus, S.E., Haeger, A., Ordaz-Ortiz, J.J. and Knox, J.P. (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohyd. Res. 344, 1858-1862.
Vesala, T., Sevanto, S., Grönholm, T., Salmon, Y., Nikinmaa, E., Hari, P. and Hölttä, T. (2017) Effect of leaf water potential on internal humidity and CO2 dissolution: reverse transpiration and improved water use efficiency under negative pressure. Front. Plant Sci. 8, 1-10.
Zimmermann, D., Westhoff, M., Zimmermann, G. et al. (2007) Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements. Protoplasma, 232, 11-34.