Plant Cell Environ. 2021 Sep;44(9):2925-2937. doi: 10.1111/pce.14129. Epub 2021 Jul 08.

Foliar water uptake via cork warts in mangroves of the Sonneratia genus.

Plant, cell & environment

Callum Bryant, Tomas I Fuenzalida, Alonso Zavafer, Hoa T Nguyen, Nigel Brothers, Rosalie J Harris, Holly A A Beckett, Helen I Holmlund, Oliver Binks, Marilyn C Ball

PMID: 34118083 DOI: 10.1111/pce.14129

Abstract

Foliar water uptake (FWU) occurs in plants of diverse ecosystems; however, the diversity of pathways and their associated FWU kinetics remain poorly resolved. We characterized a novel FWU pathway in two mangrove species of the Sonneratia genus, S. alba and S. caseolaris. Further, we assessed the influence of leaf wetting duration, wet-dry seasonality and leaf dehydration on leaf conductance to surface water (K

© 2021 John Wiley & Sons Ltd.

Keywords: dehydration; kinetics; pathway; sclereids; seasonality; surface conductance

References

1. Ball, M. C. (1988). Salinity tolerance in the mangroves Aegiceras corniculatum and Avicennia marina. I. Water use in relation to growth, carbon partitioning, and salt balance. Functional Plant Biology, 15, 447-464. - PubMed
2. 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. - PubMed
3. Benzing, D. H., & Burt, K. M. (1970). Foliar permeability among twenty species of the Bromeliaceae. Bulletin of the Torrey Botanical Club, 97, 269. - PubMed
4. Berry, Z. C., Emery, N. C., Gotsch, S. G., & Goldsmith, G. R. (2019). Foliar water uptake: Processes, pathways, and integration into plant water budgets. Plant, Cell & Environment, 42, 410-423. - PubMed
5. Binks, O., Coughlin, I., Mencuccini, M., & Meir, P. (2020). Equivalence of foliar water uptake and stomatal conductance? Plant, Cell & Environment, 43, 524-528. - PubMed
6. Binks, O., Meir, P., Rowland, L., Costa, A. C. L., da 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. - PubMed
7. Binks, O., Mencuccini, M., Rowland, L., Costa, A. C. L., da Carvalho, C. J. R., de Bittencourt, P., … Meir, P. (2019). Foliar water uptake in Amazonian trees: Evidence and consequences. Global Change Biology, 25, 2678-2690. - PubMed
8. Breshears, D. D., McDowell, N. G., Goddard, K. L., Dayem, K. E., Martens, S. N., Meyer, C. W., & Brown, K. M. (2008). Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology, 89, 41-47. - PubMed
9. Brodribb, T. J. (2015). Bringing anatomy back into the equation. Plant Physiology, 168, 1461-1461. - PubMed
10. Brodribb, T. J., & Holbrook, N. M. (2003). Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology, 132, 2166-2173. - PubMed
11. Brodribb, T. J., & Holbrook, N. M. (2005). Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology, 137, 1139-1146. - PubMed
12. Bryant, C., Fuenzalida, T. I., Brothers, N., Mencuccini, M., Sack, L., Binks, O., & Ball, M. C. (2021). Shifting access to pools of shoot water sustains gas exchange and increases stem hydraulic safety during seasonal atmospheric drought. Plant, Cell & Environment, 1-14. https://doi.org/10.1111/pce.14080 - PubMed
13. Buckley, T. N., John, G. P., Scoffoni, C., & Sack, L. (2015). How does leaf anatomy influence water transport outside the xylem? Plant Physiology, 168, 1616-1635. - PubMed
14. Burkhardt, J. (2010). Hygroscopic particles on leaves: Nutrients or desiccants? Ecological Monographs, 80, 369-399. - PubMed
15. Burkhardt, J., Basi, S., Pariyar, S., & Hunsche, M. (2012). Stomatal penetration by aqueous solutions-An update involving leaf surface particles. New Phytologist, 196, 774-787. - PubMed
16. Byrt, C. S., Zhao, M., Kourghi, M., Bose, J., Henderson, S. W., Qiu, J., … Tyerman, S. (2017). Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant, Cell & Environment, 40, 802-815. - PubMed
17. Cavallaro, A., Carbonell, S. L., Pereyra, D. A., Goldstein, G., Scholz, F. G., & Bucci, S. J. (2020). Foliar water uptake in arid ecosystems: seasonal variability and ecophysiological consequences. Oecologia, 193, 337-348. - PubMed
18. Chaumont, F., & Tyerman, S. D. (2014). Aquaporins: Highly regulated channels controlling plant water relations. Plant Physiology, 164, 1600-1618. - PubMed
19. Chiang, J.-M., Lin, T.-C., Luo, Y.-C., Chang, C.-T., Cheng, J.-Y., & Martin, C. E. (2013). Relationships among rainfall, leaf hydrenchyma, and Crassulacean acid metabolism in Pyrrosia lanceolata (L.) Fraw. (Polypodiaceae) in Central Taiwan. Flora-Morphology, Distribution, Functional Ecology of Plants, 208, 343-350. - PubMed
20. Coopman, R. E., Nguyen, H. T., Mencuccini, M., Oliveira, R. S., Sack, L., Lovelock, C. E., & Ball, M. C. (2021). Harvesting water from unsaturated atmospheres: Deliquescence of salt secreted onto leaf surfaces drives reverse sap flow in a dominant arid climate mangrove, Avicennia Marina. New Phytologist. https://doi.org/10.1111/nph.17461 - PubMed
21. Dawson, T. E., & Goldsmith, G. R. (2018). The value of wet leaves. New Phytologist, 219, 1156-1169. - PubMed
22. Duke, N. C. (1992). Chapter 4 - Mangrove floristics and biogeography. In Robertson, A., & Alongi, D. (Eds.), Tropical Mangrove Ecosystems, (pp. 63-100). Washington, DC: the American Geophysical Union. - PubMed
23. Duke, N., Ball, M., & Ellison, J. (1998). Factors influencing biodiversity and distributional gradients in mangroves. Global Ecology & Biogeography Letters, 7, 27-47. - PubMed
24. 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. - PubMed
25. Eller, C. B., Lima, A. L., & 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 Phytologist, 211, 489-501. - PubMed
26. Evans, L. S., & Bromberg, A. (2010). Characterization of cork warts and aerenchyma in leaves of Rhizophora mangle and Rhizophora racemosa. The Journal of the Torrey Botanical Society, 137, 30-38. - PubMed
27. Evans, L. S., Testo, Z. M., & Cerutti, J. A. (2009). Characterization of internal airflow within tissues of mangrove species from Australia: Leaf pressurization processes. The Journal of the Torrey Botanical Society, 136, 70-83. - PubMed
28. Evert, R. F. (2006). Esau's plant anatomy: Meristems, cell and tissues of the plant body: Their structure, function, and development (3rd ed.). Hoboken, NJ: John Wiley & Sons. - PubMed
29. Ewing, H. A., Weathers, K. C., Templer, P. H., Dawson, T. E., Firestone, M. K., Elliott, A. M., & Boukili, V. K. S. (2009). Fog water and ecosystem function: Heterogeneity in a California redwood Forest. Ecosystems, 12, 417-433. - PubMed
30. Farooqui, P. (1982). Cork-warts in Eucalyptus species. Proc. Indian Acad. Sci. (Plant Sci.), 91(4), 289-295. - PubMed
31. Fernández, V., Bahamonde, H. A., Javier, P.-P. J., Gil-Pelegrín, E., Sancho-Knapik, D., Gil, L., … Eichert, T. (2017). Physico-chemical properties of plant cuticles and their functional and ecological significance. Journal of Experimental Botany, 68, 5293-5306. - PubMed
32. Flowers, T. J., & Colmer, T. D. (2008). Salinity tolerance in halophytes. The New Phytologist, 179, 945-963. - PubMed
33. Foster, A. S. (1956). Plant idioplasts: Remarkable examples of cell specialization. Protoplasma, 46, 184-193. - PubMed
34. Fuenzalida, T. I., Bryant, C. J., Ovington, L. I., Yoon, H.-J., Oliveira, R. S., Sack, L., & Ball, M. C. (2019). Shoot surface water uptake enables leaf hydraulic recovery in Avicennia marina. New Phytologist, 224, 1504-1511. - PubMed
35. Gotsch, S. G., Nadkarni, N., Darby, A., Glunk, A., Dix, M., Davidson, K., & Dawson, T. E. (2015). Life in the treetops: Ecophysiological strategies of canopy epiphytes in a tropical montane cloud forest. Ecological Monographs, 85, 393-412. - PubMed
36. Griffith, M. M. (1968). The structure and development of foliar sclereids in Osmanthus fragrans Lour. Phytomorphology, 18, 75-79. - PubMed
37. Guzmán-Delgado, P., Earles, J. M., & Zwieniecki, M. A. (2018). Insight into the physiological role of water absorption via the leaf surface from a rehydration kinetics perspective. Plant, Cell & Environment, 41, 1886-1894. - PubMed
38. Guzmán-Delgado, P., Laca, E., & Zwieniecki, M. A. (2021). Unravelling foliar water uptake pathways: The contribution of stomata and the cuticle. Plant, Cell & Environment, 44, 1728-1740. - PubMed
39. Heide-Jorgensen, H. S. (1990). Xeromorphic leaves of Hakea suaveolens R. Br. IV. Ontogeny, structure and function of the Sclereids. Australian Journal of Botany, 38, 25-43. - PubMed
40. Joffily, A., & Cardoso, V. R. (2010). Cork-warts on the leaf epidermis of four genera of Celastroidea-Celastraceae. Flora-Morphology, Distribution, Functional Ecology of Plants, 205, 313-318. - PubMed
41. Korn, R. W., & Fredrick, G. W. (1973). Development of D-type stomata in the leaves of Ilex crenata var. convexa. Annals of Botany, 37(3), 647-656. - PubMed
42. Kourghi, M., Pei, J. V., Ieso, M. L. D., Nourmohammadi, S., Chow, P. H., & Yool, A. J. (2018). Fundamental structural and functional properties of aquaporin ion channels found across the kingdoms of life. Clinical and Experimental Pharmacology and Physiology, 45, 401-409. - PubMed
43. Limm, E. B., Simonin, K. A., Bothman, A. G., & Dawson, T. E. (2009). Foliar water uptake: A common water acquisition strategy for plants of the redwood forest. Oecologia, 161, 449-459. - PubMed
44. Losada, J. M., Díaz, M., & Holbrook, N. M. (2020). Idioblasts and peltate hairs as distribution networks for water absorbed by xerophilous leaves. Plant, Cell & Environment, 44(5), 1346-1360. - PubMed
45. Malaviya, M. (1976). On the occurence of sclereids in two genera of Myrtaceae. Proceedings of the Indian Academy of Sciences-Section B, 66, 45-52. - PubMed
46. Martin, C. E., & 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 Biology, 2, 229-242. - PubMed
47. Moon, G. J., Clough, B. F., Peterson, C. A., & Allaway, W. G. (1986). Apoplastic and symplastic pathways in Avicennia marina (Forsk.) Vierh. Roots revealed by fluorescent tracer dyes. Functional Plant Biology, 13, 637-648. - PubMed
48. Nguyen, H. T., Meir, P., Wolfe, J., Mencuccini, M., & Ball, M. C. (2017). Plumbing the depths: Extracellular water storage in specialized leaf structures and its functional expression in a three-domain pressure-volume relationship. Plant, Cell & Environment, 40, 1021-1038. - PubMed
49. Nguyen, H. T., Stanton, D. E., Schmitz, N., Farquhar, G. D., & Ball, M. C. (2015). Growth responses of the mangrove Avicennia marina to salinity: Development and function of shoot hydraulic systems require saline conditions. Annals of Botany, 115, 397-407. - PubMed
50. Nonami, H., & Schulze, E.-D. (1989). Cell water potential, osmotic potential, and turgor in the epidermis and mesophyll of transpiring leaves. Planta, 177, 35-46. - PubMed
51. Oliveira, R. S., Eller, C. B., Bittencourt, P. R. L., & Mulligan, M. (2014). The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Annals of Botany, 113, 909-920. - PubMed
52. Passioura, J. B., Ball, M. C., & Knight, J. H. (1992). Mangroves may salinize the soil and in so doing limit their transpiration rate. Functional Ecology, 6, 476. - PubMed
53. 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/. - PubMed
54. Rao, A. N., & Chin, W. Y. (1966). Foliar sclereids in certain members of Annonaceae and Myristicaceae. Flora oder Allgemeine botanische Zeitung. Abt. A, Physiologie Und Biochemie, 156, 220-231. - PubMed
55. Rao, A. T., & Mody, K. J. (1961). On terminal sclereids and tracheoid idioblasts. Proceedings of the Indian Academy of Sciences-Section B, 53, 257-262. - PubMed
56. Rao, T. A., & Bhupal, O. P. (1973). Typology of sclereids. Proceedings of the Indian Academy of Sciences-Section B, 77, 41-55. - PubMed
57. Raux, P. S., Gravelle, S., & Dumais, J. (2020). Design of a unidirectional water valve in Tillandsia. Nature Communications, 11, 396. - PubMed
58. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., … Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676-682. - PubMed
59. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. - PubMed
60. Schönherr, J., & Bukovac, M. J. (1972). Penetration of stomata by liquids: Dependence on surface tension, wettability, and stomatal morphology. Plant Physiology, 49, 813-819. - PubMed
61. Schreel, J. D. M., & Steppe, K. (2020). Foliar water uptake in trees: Negligible or necessary? Trends in Plant Science, 25, 590-603. - PubMed
62. Schreel, J. D. M., Van de Wal, B. A. E., Hervé-Fernandez, P., Boeckx, P., & Steppe, K. (2019). Hydraulic redistribution of foliar absorbed water causes turgor-driven growth in mangrove seedlings. Plant, Cell & Environment, 42, 2437-2447. - PubMed
63. Schreel, J. D. M., von der Crone, J. S., Kangur, O., & Steppe, K. (2019). Influence of drought on foliar water uptake capacity of temperate tree species. Forests, 10, 562. - PubMed
64. Stadelmann, E. J., & Kinzel, H. (1972). Vital staining of plant cells. In D. M. Prescott (Ed.), Methods in cell biology (pp. 325-372). New York: Academic Press. - PubMed
65. Steppe, K., Vandegehuchte, M. W., Van de Wal, B. A. E., Hoste, P., Guyot, A., Lovelock, C. E., & Lockington, D. A. (2018). Direct uptake of canopy rainwater causes turgor-driven growth spurts in the mangrove Avicennia marina. Tree Physiology, 38, 979-991. - PubMed
66. Tan, W.-K., Lin, Q., Lim, T.-M., Kumar, P., & Loh, C.-S. (2013). Dynamic secretion changes in the salt glands of the mangrove tree species Avicennia officinalis in response to a changing saline environment. Plant, Cell & Environment, 36, 1410-1422. - PubMed
67. Tomlinson, P. B. (1959). Structure and distribution of sclereids in the leaves of palms. New Phytologist, 58, 253-266. - PubMed
68. Tomlinson, P. B. (1986). The botany of mangroves. Cambridge, UK: Cambridge University Press. - PubMed
69. Tyree, M. T., & Tammes, P. M. L. (1975). Translocation of uranin in the symplasm of staminal hairs of Tradescantia. Canadian Journal of Botany, 53, 2038-2046. - PubMed
70. Vesala, T., Sevanto, S., Grönholm, T., Salmon, Y., Nikinmaa, E., Hari, P., & Hölttä, T. (2017). Effect of leaf water potential on internal humidity and CO2 dissolution: Reverse transpiration and improved water use efficiency under negative pressure. Frontiers in Plant Science, 8, 54. - PubMed
71. Wang, X., Xiao, H., Cheng, Y., & Ren, J. (2016). Leaf epidermal water-absorbing scales and their absorption of unsaturated atmospheric water in Reaumuria soongorica, a desert plant from the northwest arid region of China. Journal of Arid Environments, 128, 17-29. - PubMed
72. Yan, X., Zhou, M., Dong, X., Zou, S., Xiao, H., & Ma, X.-F. (2015). Molecular mechanisms of foliar water uptake in a desert tree. AoB PLANTS, 7, plv129. - PubMed
73. Yates, D., & Hutley, L. (1995). Foliar uptake of water by wet leaves of Sloanea woollsii, an Australian subtropical rainforest tree. Australian Journal of Botany, 43, 157. - PubMed

Publication Types

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