Keywords
leaf micromorphology
silicon
laser confocal microscopy
scanning electron microscopy
shade influence
How to Cite
Abstract
The micromorphology of the leaf epidermis, localization, and silicon content in the epidermal cells of Quercus robur leaves growing in the shade and under direct sunlight in the Feofaniya Park (Kyiv, Ukraine) were studied using scanning electron microscopy and laser confocal microscopy. Silicon inclusions were found in the anticlinal and periclinal walls of adaxial epidermal cells, trichomes, guard cells of stomata, and walls of regular epidermal cells on the abaxial leaf surface, the amount of which varied according to the conditions of growth. Natural shading and the intensity of solar irradiation were found affecting the size of leaf blades, the ultrastructure of the leaf epidermis, and changes in the silicon content of oak leaves. Studies have shown that the anticlinal walls of the adaxial epidermis and the trichomes and stomata of the abaxial epidermis of leaves are the main silicon accumulators. The findings suggest that changes in leaf microstructure and silicon content contribute to maintaining optimal water balance in plants and can be regarded as signs of phenotypic plasticity in plants and an adaptive marker depending on the sunlight conditions of oak growth.
References
Aseeva, T.A., Batuev, B.B., Khapkin, S., Fedotovskikh, N.N., & Datiev, D.V. (1985). Study of Tibetan multi-component medicinal mixtures. Plant Resources, 21(1), 15–25. (In Russian)
Bacelar, E.A., Correia, C.M., Moutinho-Pereira, J.M., Goncalves, B.C., Lopes, J.L., & Torres-Pereira, J.M.G. (2004). Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiology, 24(2), 233–239. https://doi.org/10.1093/treephys/24.2.233
Barlott, W., Mail, M., Bhuchan, B., & Koch, K. (2017). Plant surface: structures and functions for biomimetic innovations. Nano-Micro Letters, 9(2), Article 23. https://doi.org/10.1007/s40820-016-0125-1
Bashir, L. (2022). Stomata density in shade vs sun leaves. BIOL151: Principles of Biology II. https://info.montgomerycollege.edu/_documents/resources/writing-in-the-disciplines/layann-bashir-2021-2022.pdf
Bickford, C.P. (2016). Eco-physiology of leaf trichomes. Functional Plant Biology, 43(9), 807–814. https://doi.org/10.1071/FP16095
Björkman, O. (1981). Responses to different quantum flux densities. In O.L. Lange, P.S. Nobel, C.B. Osmond & H. Zeigler (Eds.), Physiological Plant Ecology I. Encyclopedia of Plant Physiology. Vol. 12 (pp. 47–107). Springer, Berlin – New York. https://doi.org/10.1007/978-3-642-68090-8_4
Björkman, O., & Powles S.B. (1981). Leaf movement in the shade species Oxalis oregana. I. Response to light level and light quality. Carnegie Institute of Washington Year Book. Series B, 80, 59–62.
Bolhar-Nordenkampf, H. (1987). Shoot morphology and leaf anatomy in relation to photosynthesis. In J. Coombs, D. Hall, S. Long & J. Scurlock (Eds.), Techniques in bioproductivity and photosynthesis (pp. 107–117). Pergamon Press, Oxford.
Brugnoli E., & Björkman O. (1992). Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynthesis Research, 32, 23–35. https://doi.org/10.1007/BF00028795
Chaves, M.M., Pereira, J.S., Maroco, J., Rodrigues, M.L., Ricardo, C.P.P., Osório, M.L., Carvalho, I., Faria, T., & Pinheiro, C. (2002). How plants cope with water stress in the field? Photosynthesis and growth. Annals of Botany, 89(7), 907–916. https://doi.org/10.1093/aob/mcf105
Coder, K.D. (2010). Tree trichomes: Big hairy tree? Warnell School University of Georgia, Article WSFNR-20-45C. https://urbanforestrysouth.org/resources/library/citations/Citation.2004-07-16.2805
Custódio, L., Patarra, J., Albeґício, F., Neng, N.D.R., Nogueira, J.M.F., & Romano, A. (2015). Phenolic composition, antioxidant potential and in vitro inhibitory activity of leaves and acorns of Quercus ruber on key enzymes relevant for hyperglycemia and Alzheimer’s disease. Industrial Crops and Products, 64, 45–51. https://doi.org/10.1016/j.indcrop.2014.11.001
Dabney, C., Ostergaard, J., Watkins, E., & Chen, C. (2016). A novel method to characterize silica bodies in grasses. Plant Methods, 12, 3–10. https://doi.org/10.1186/s13007-016-0108-8
Dietz, K.-J., & Hartung, W. (1996). The leaf epidermis: its ecophysiological significance. Progress in Botany / Fortschritte der Botanik, 57, 32–53. https://doi.org/10.1007/978-3-642-79844-3_3
Granier, C., & Tardieu, F. (1999). Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in the sunflower leaf. Plant, Cell & Environment, 22(11), 1365–1376. https://doi.org/10.1046/j.1365-3040.1999.00497.x
Grašič, M., Sakovič, D., Abram, K., Vogel-Mikuš, K., & Gaberščik, A. (2020). Do soil and leaf silicon content affect leaf functional traits in Deshampsia caespitosa from different habitats? Biologia Plantarum, 64(130), 234–243. https://doi.org/10.32615/bp.2019.155
Guerriero, G., Hausman, J.F., & Legay, S. (2016). Silicon and the plant extracellular matrix. Frontiers in Plant Science, 7, Article 463. https://doi.org/10.3389/fpls.2016.00463
Hansen, D.L., Lambertini, C., Jampeetong, A., & Brix, H. (2007). Clone-specific differences in Phragmites australis: effects of ploidy level and geographic origin. Aquatic Botany, 86(3), 269–279. https://doi.org/10.1016/j.aquabot.2006.11.005
Hardin, J.W. (1976). Terminology and classification of Quercus trichomes. Journal of Elisha Mitchell Science Society, 92, 151–161.
Hetherington, A.M., & Woodward, F.I. (2003). The role of stomata in sensing and driving environmental change. Nature, 424, 901–908. https://doi.org/10.1038/nature01843
Hofmeister, M., Pitman, K.M., Goncharov, A., & Speck, A. (2009). Optical constants of silicon carbide for astrophysical appplications. II. Extending optical functions from infrared to ultraviolet using single crystal absorption spectra. The Astrophysical Journal, 696(2), 1502–1516. https://doi.org/10.1088/0004-637X/696/2/1502
Karabourniotis, G., Liakopoulos, G., Nikolopoulos, D., & Bresta, P. (2020). Protective and defensive roles of non‑glandular trichomes against multiple stresses: structure–function coordination. Journal of Forestry Research, 31, 1–12. https://doi.org/10.1007/s11676-019-01034-4
Kardiman, R., & Ræbild, A. (2018). Relationship between stomatal density, size and speed of opening in Sumatran rainforest species. Tree Physiology, 38(5), 696–705. https://doi.org/10.1093/treephys/tpx149
Kerstiens, G. (1996). Cuticular water permeability and its physiological significance. Journa of Experimental Botany, 47(12), 1813–1832. https://doi.org/10.1093/jxb/47.12.1813
Kolesnikov, M.P., & Gins, V.K. (2001). Forms of silicon in medicinal plants. Applied Biochemistry and Microbiology, 37(5), 524–527. https://doi.org/10.1023/A:1010262527643
Larcher, W. (1960). Transpiration and photosynthesis of detached leaves and shoots of Quercus pubescens and Quercus ilex during desiccation under standard conditions. Bulletin of the Research Council of Israel, 8D(3–4), 213–224.
Larcher, W. (2003). Physiological plant ecology. Ecophysiology and stress physiology of functional groups. Springer. https://link.springer.com/book/9783540435167
Leandro, T.D., Shirasuna, R.T., Filgueiras, T.S., & Scatena, V.L. (2016). The utility of Bambusoideae (Poaceae, Poales) leaf blade anatomy for identification and systematics. Brazilian Journal of Biology, 76(3), 708–717. https://doi.org/10.1590/1519-6984.01715
Leon, J.M., & Bukovac, M. (1978). Cuticle development and surface morphology of olive leaves with reference to penetration of foliar-applied chemicals. Journal of the American Society for Horticular Science, 103(4), 465–472. https://doi.org/10.21273/JASHS.103.4.465
Liakoura, V., Stavrianakou, S., Liakopoulos, G., Karabourniotis, G., & Manetas, Y. (1999). Effects of UV-B radiation on Olea europaea: comparisons between a greenhouse and a field experiment. Tree Physiol, 19(13), 905–908. https://doi.org/10.1093/treephys/19.13.905
Lins, U., Barros, C.F., da Cunha, M., & Miguens, F.C. (2002). Structure, morphology and composition of silicon biocomposites in the palm tree Syagrus coronate (Mart.) Becc. Protoplasma, 220(1–2), 89–96. https://doi.org/10.1007/s00709-002-0036-5
Liu, Y., Dawson, W., Prati, D., Haeuser, E., Feng, Y., & van Kleunen, M. (2016). Does greater specific leaf area plasticity help plants to maintain a high performance when shaded? Annals of Botany, 118(7), 1329–1336. https://doi.org/10.1093/aob/mcw180
Llamas, F., Perez-Morales, C., Acedo, C., & Penas, A. (1995). Foliar trichomes of the evergreen and semi-deciduous species of the genus Quercus (Fagaceaea) in the Iberian penisula. Botanical Journal of the Linnean Sociey, 117(1), 47–57. https://doi.org/10.1111/j.1095-8339.1995.tb02377.x
LoPresti, E.F. (2015). Chemicals on plant surfaces as a heretofore unrecognized, but ecologically informative, class for investigations into plant defence. Biological Reviews, 91(4), 1102–1117. https://doi.org/10.1111/brv.12212
Ma, F.J., Yamaji, N., & Mitani-Ueno, N. (2011). Transport of silicon from roots to panicles in plants. Proceedings of the Japan Academy. Series B, 87(7), 377–385. https://doi.org/10.2183/pjab.87.377
Mathur, S., Jain, L., & Jajoo, A. (2018). Photosynthetic efficiency in sun and shade plants. Photosynthetica, 56(1), 354–365. https://doi.org/10.1007/s11099-018-0767-y
Matos, F.S., Wolfgramm, R., Gonçalves, F.V., Cavatte, P.C., Ventrella, M.C., & DaMatta, F.M. (2009). Phenotypic plasticity in response to light in the coffee tree. Environmental and Experimental Botany, 67(2), 421–427. https://doi.org/10.1016/j.envexpbot.2009.06.018
Mirshafieyan, S.A., & Guo, J. (2014). Silicon colors: spectral selective perfect light absorption in single layer silicon films on aluminum surface and its thermal tenability. Optics Express, 22(25), 31545–31554. https://doi.org/10.1364/OE.22.031545
Moon, H.R., Chung, M., Park, J.W., Сho, S.M., Choi, D.J., Kim, S.M., Chun, M.H., Kim, I.B., Kim, S.G., Jang, S.J., & Park, Y. (2013). Antiasthma effects through anti-inflammatory action of acorn (Quercus acutissima Carr.) in vitro and in vivo. Journal of Food Biochemistry, 37(1), 108–118. https://doi.org/10.1111/j.1745-4514.2012.00652.x
Müller, W.E.G., & Grachev, M.A. (2009). Biosilica in evolution, morphogenesis, and nano-biotechnology. In W.E.G. Müller & M.A. Grachev (Eds.), Progress in molecular and subcellular biology. Vol. 47 (pp. 1–421). Springer Verlag, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88552-8
Nevo, E., Bolshakova, M.A., Martyn, G.I., Musatenko, L.I., & Sytnik, K.M. (2013). Drought and light anatomical adaptive leaf strategies in three woody species caused by microclimatic selection at Evolution Canyon, Israel. Israel Journal of Plant Sciences, 48(1), 33–46. https://doi.org/10.1560/RNPF-9HJE-8J3L-B5F1
Nicolić, N., Merkulov, L.S., Krstić, B.D., & Orlović, S.S. (2003). A comparative analysis of stomata and leaf trichome characteristics in Quercus robur L. genotypes. Proceedings for Natural Sciences, Matica Srpska, Novi Sad, 105, 51–59. https://doi.org/10.2298/ZMSPN0305051N
Niinemets, Ü., & Sack, L. (2006). Structural determinants of leaf light harvesting capacity and photosynthetic potentials. In K. Esser, U. Lüttge, W. Beyschlag & J. Murata (Eds.), Progress in Botany. Vol. 67 (pp. 385–419). https://doi.org/10.1007/3-540-27998-9_17
Onoda, Y., Schieving, F., & Anten, N.P. (2008). Effects of light and nutrient availability on leaf mechanical properties of Plantago major: a conceptual approach. Annals of Botany, 101(5), 727–736. https://doi.org/10.1093/aob/mcn013
Onwueme, I.C., & Johnston, M. (2000). Influence of shade on stomatal density, leaf size and other leaf characteristics in the major tropical root crops, tannia, sweet potato, yam, cassava and taro. Experimental Agriculture, 36(4), 509–516. https://doi.org/10.1017/S0014479700001071
Raven, J.A. (2014). Speedy small stomata? Journal of Experimental Botany, 65(6), 1415–1424. https://doi.org/10.1093/jxb/eru032
Richardson, A.D., & Berlyn, G.P. (2002). Changes in foliar spectral reflectance and chlorophyll fluorescence of four temperate species following branch cutting. Tree Physiology, 22(7), 499–506. https://doi.org/10.1093/treephys/22.7.499
Sanson, G., Read, J., Aranwela, N., Clissold, F., & Peeters, P. (2001). Measurement of leaf biomechanical properties in studies of herbivory: opportunities, problems and procedures. Austral Ecology, 26(5), 535–546. https://doi.org/10.1046/j.1442-9993.2001.01154.x
Soares, J.D.R., Pasqual, M., de Araujo, A.G., de Castro, E.M., Pereira, F.J., & Braga, F.T. (2012). Leaf anatomy of orchids micropropagated with different silicon concentrations. Acta Scientiarum Agronomy, 34(4), 413–421. https://doi.org/10.4025/actasciagron.v34i4.15062
Tahir, N.A.R., Rasul, K.S., Lateef, D.D., & Grundler, F.M. (2022). Effects of oak leaf extract, biofertilizer, and soil containing oak leaf powder on tomato growth and biochemical characteristics under water stress conditions. Agriculture, 12(12), Article 2082. https://doi.org/10.3390/agriculture12122082
Taib, M., Rezzak, Y., Bouyazza, L., & Lyoussi, B. (2020). Medicinal uses, phytochemistry, and pharmacological activities of Quercus species. Hindawi Evidence-Based Complementary and Alternative Medicine, 2020, Article 1920683. https://doi.org/10.1155/2020/1920683
Talbot, M., & White, R. (2013). Cell surface and cell outline imaging in plant tissues using the backscattered electron detector in a variable pressure scanning electron microscope. Plant Methods, 9, Article 40. https://doi.org/10.1186/1746-4811-9-40
Terashima, I., Hanba, Y.T., Tazoe, Y., Vyas, P., & Yano, S. (2006). Irradiance and phenotype: Comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. Journal of Experimental Botany, 57(2), 343–354. https://doi.org/10.1093/JXB%2FERJ014
Vatnick, I., & Bruce, W. (2004). Environmental correlates of leaf stomata density (Synopsis). Teaching Issues and Experiments in Ecology, 1, 1–24. https://tiee.esa.org/vol/v1/experiments/stomata/pdf/stomata.pdf
Wang, L., Nie, Q., Li, M., Zhang, F., Zhuang, J., & Yang, W. (2005). Biosilicified structures for cooling plant leaves: a mechanism of highly efficient mid in frared thermal emission. Applied Physics Letters, 87(19), Article 194105. https://doi.org/10.1063/1.2126115
Werker, E. (2000). Trichome diversity and development. Advances in Botanical Research, 31(1), 1–35. https://doi.org/10.1016/S0065-2296(00)31005-9
Wu, Y., Gong, W., & Yang, W. (2017). Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean. Scientific Reports, 7(1), Article 9259. https://doi.org/10.1038/s41598-017-10026-5
Yahaya, N. A., Yamada, N., Kotaki, Y., & Nakayama, T. (2013). Characterization of light absorption in thin-film silicon with periodic nanohole arrays. Optics Express, 21(5), 5924–5930. https://doi.org/10.1364/OE.21.005924
Yamasaki, S., & Murakami, Y. (2014). Continuous UV-B irradiation induces endoreduplication and trichome formation in cotyledon and reduces epidermal cell division and expansion in the first leaves of pumpkin seedlings (Cucurbita maxima Duch. × C. moschata Duch.). Environmental Control in Biology, 52(4), 203–209. https://doi.org/10.2525/ecb.52.203
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