Abstract
While increasing numbers of studies report wide variations of leaf silicon (Si) accumulation among plant species, within-species variations of leaf Si accumulation have scarcely been examined for tree species. As in crop plants, environmental factors that affect transpiration rates may influence passive transpiration-dependent transport of Si uptake in trees. Here, we tested a hypothesis that leaf Si accumulation rate should be higher in shoots that receive more light and thus achieve faster growth, using Broussonetia papyrifera, a pioneer tree species with successive leaf production and Si accumulation with leaf age. We marked individual leaves weekly throughout the growing season (June–September), and measured Si concentration and light availability in relation to the chronosequence of leaf age in September. In shoots that continued growing and successively produced leaves throughout the growing season, leaf Si content increased linearly with leaf age. In support of our hypothesis, leaf Si accumulation rate varied widely among shoots with positive correlations with shoot growth and light availability. In conclusion, both leaf age and microenvironment affect within-species variations in leaf Si concentration of this species, a moderate Si accumulator.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Conley DJ, Schelske CL (1993) Potential role of sponge spiculesin influencing the silicon biogeochemistry of Florida lakes. Can J Fish Aquat Sci 50:296–302. https://doi.org/10.1139/f93-034
Cooke J, Leishman MR (2016) Consistent alleviation of abiotic stress with silicon addition: a meta-analysis. Funct Ecol 30:1340–1357. https://doi.org/10.1111/1365-2435.12713
Cornelis JT, Ranger J, Iserentant A, Delvaux B (2010) Tree species impact the terrestrial cycle of silicon through various uptakes. Biogeochemistry 97:231–245. https://doi.org/10.1007/s10533-009-9369-x
Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The controversies of silicon’s role in plant biology. New Phytol 221:67–85. https://doi.org/10.1111/nph.15343
Datnoff LE, Snyder GH, Korndörfer GH (2001) Silicon in agriculture. Elsevier, Amsterdam
Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17. https://doi.org/10.1073/pnas.91.1.11
Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol. https://doi.org/10.1146/annurev.arplant.50.1.641
Faisal S, Callis KL, Slot M, Kitajima K (2012) Transpiration-dependent passive silica accumulation in cucumber (Cucumis sativus) under varying soil silicon availability. Botany 90:1058–1064. https://doi.org/10.1139/b2012-072
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Granier A (1985) Une nouvelle méthod pour la measure de flux de sève brute dans le tronc des arbres. Ann Sci Forest 42:81–88
Henriet C, Draye X, Oppitz I, Swennen R, Delvaux B (2006) Effects, distribution and uptake of silicon in banana (Musa spp.) under controlled conditions. Plant Soil 287:359–374. https://doi.org/10.1007/s11104-006-9085-4
Ishizawa H, Niiyama K, Iida Y, Shari NHZ, Ripin A, Kitajima K (2019) Spatial variations of soil silicon availability and biogenic silicon flux in a lowland tropical forest in Malaysia. Ecol Res 34:548–559. https://doi.org/10.1111/1440-1703.12025
Kitajima K, Mulkey SS, Samaniego M, Wright SJ (2002) Decline of photosynthetic capacity with leaf age and position in two tropical pioneer tree species. Am J Bot 89:1925–1932. https://doi.org/10.3732/ajb.89.12.1925
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linearmixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Liang Y, Si J, Römheld V (2005) Silicon uptake and transport is an active process in Cucumis sativus. New Phytol 167:797–804. https://doi.org/10.1111/j.1469-8137.2005.01463.x
Liang Y, Hua H, Zhu YG, Zhang J, Cheng C, Römheld V (2006) Importance of plant species and external silicon concentration to active silicon uptake and transport. New Phytol 172:63–72. https://doi.org/10.1111/j.1469-8137.2006.01797.x
Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18. https://doi.org/10.1080/00380768.2004.10408447
Ma JF, Takahashi E (2002) Soil, fertilizer and plant silicon research in Japan. Elsevier, Amsterdam
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691. https://doi.org/10.1038/nature04590
Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212. https://doi.org/10.1038/nature05964
Mayland HF, Wright JL, Sojka RE (1991) Silicon accumulation and water uptake by wheat. Plant Soil 137:191–199. https://doi.org/10.1007/BF00011197
Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 56:1255–1261. https://doi.org/10.1093/jxb/eri121
Mitani N, Ma JF, Iwashita T (2005) Identification of the silicon form in xylem sap of rice (Oryza sativa L.). Plant Cell Physiol 46:279–283. https://doi.org/10.1093/pcp/pci018
Motomura H, Mita N, Suzuki M (2002) Silica accumulation in long-lived leaves of Sasa veitchii (Carrière) rehder (Poaceae-Bambusoideae). Ann Bot 90:149–152. https://doi.org/10.1093/aob/mcf148
Motomura H, Fujii T, Suzuki M (2004) Silica deposition in relation to ageing of leaf tissues in Sasa veitchii (Carrière) Rehder (Poaceae: Bambusoideae). Ann Bot 93:235–248. https://doi.org/10.1093/aob/mch034
Motomura H, Fujii T, Suzuki M (2006) Silica deposition in abaxial epidermis before the opening of leaf blades of Pleioblastus chino (Poaceae, Bambusoideae). Ann Bot 97:513–519. https://doi.org/10.1093/aob/mcl014
Motomura H, Hikosaka K, Suzuki M (2008) Relationships between photosynthetic activity and silica accumulation with ages of leaf in Sasa veitchii (Poaceae, Bambusoideae). Ann Bot 101:463–468. https://doi.org/10.1093/aob/mcm301
Nakamura R, Ishizawa H, Wagai R, Suzuki S, Kitayama K, Kitajima K (2019) Silicon cycled by tropical forest trees: effects of species, elevation and parent material on Mount Kinabalu, Malaysia. Plant Soil 443:155–166. https://doi.org/10.1007/s11104-019-04230-7
Nakamura R, Cornelis JT, de Tombeur F, Nakagawa M, Kitajima K (2020) Comparative analysis of borate fusion versus sodium carbonate extraction for quantification of silicon contents in plants. J Plant Res 133:271–277. https://doi.org/10.1007/s10265-019-01162-2
Okuda A, Takahashi E (1962) Studies on the plant-physiological role of silicon in crop-plant. Part 8 Some examination on the specific behavior low land rice in silicon uptake. Jpn J Soil Sci Plant Nutr 33:217–221. https://doi.org/10.20710/dojo.33.5_217 (in Japanese)
Osada N, Hiura T (2017) How is light interception efficiency related to shoot structure in tall canopy species? Oecologia 185:29–41. https://doi.org/10.1007/s00442-017-3926-0
R Development Core Team (2016) R: a language an environment for statistical computing. R Foundation for Statistical Computing, Vienna
Sauer D, Saccone L, Conley DJ, Herrmann L, Sommer M (2006) Review of methodologies for extracting plant-available and amorphous Si from soils and aquatic sediments. Biogeochemistry 80:89–108. https://doi.org/10.1007/s10533-005-5879-3
Schaller J, Turner BL, Weissflog A, Pino D, Bielnicka AW, Engelbrecht BMJ (2018) Silicon in tropical forests: large variation across soils and leaves suggests ecological significance. Biogeochemistry 140:161–174. https://doi.org/10.1007/s10533-018-0483-5
Sharkey TD, Raschke K (1981) Separation and measurement of direct and indirect effects of light on stomata. Plant Physiol 68:33–40. https://doi.org/10.1104/pp.68.1.33
Takahashi E, Ma JF, Miyake Y (1990) The possibility of silicon as an essential element for higher plants. Comments Agric Food Chem 2:99–102
Tamai K, Ma JF (2003) Characterization of silicon uptake by rice roots. New Phytol. https://doi.org/10.1046/j.1469
Umemura M, Takenaka C (2014) Biological cycle of silicon in moso bamboo (Phyllostachys pubescens) forests in central Japan. Ecol Res 29:501–510. https://doi.org/10.1007/s11284-014-1150-5
Wyttenbach A, Tobler L, Bajo S (1991) Silicon concentration in spruce needles. Zeitschrift Pflanzenernährung Bodenkd 154:253–258. https://doi.org/10.1002/jpln.19911540403
Acknowledgements
We appreciate Naoto Nakamura, Ryota Sasaki, and Shinji Yamada for supporting the fieldwork. Ryosuke Nakamura provided helpful comments on earlier drafts of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kajino, H., Kitajima, K. Leaf silicon accumulation rates in relation to light environment and shoot growth rates in paper mulberry (Broussonetia papyrifera, Moraceae). J Plant Res 134, 1013–1020 (2021). https://doi.org/10.1007/s10265-021-01326-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-021-01326-z