Abstract
Purpose
Silicon is important for both plant growth and the soil biogeochemical cycle. Si uptake and accumulation ability varies in plants, which are defined as Si accumulators, intermediates, or non-accumulators. However, the processes governing Si uptake and translocation are not fully understood. Stable Si isotopic signatures may offer new perspectives on the processes involved in the Si biogeochemical cycle.
Methods
Si isotopic fractionation between different Si pools was analyzed in Si accumulators (rice, maize), intermediates (cucumber), and non-accumulators (tomato) grown in yellow, black, and cinnamon soils using multi-collector inductively coupled plasma mass spectrometry.
Results
Plants grown in all soil types exhibited 28Si enrichment relative to the soil solution. The degree of fractionation was negatively correlated with silt, clay, free iron oxide (Fed), and crystalline Fe oxide (Fed-Feo) contents, and positively correlated with sand content. The degree of isotope fractionation was species-specific during uptake, in order of rice > maize > cucumber > tomato, while the reverse was true for root–shoot translocation. In addition, isotope fractionation was absent in tomato shoots, contrasting with the Rayleigh-like behavior of the other species.
Conclusion
Fed and Fed-Feo contents affected the H4SiO4 adsorption–desorption process, thereby influencing isotope fractionation between the plants and soil. Species-specific fractionation was attributed to the varying contributions of water flow uptake and the transporter-mediated uptake process. Moreover, the Si transport mechanism within shoots in Si non-accumulators varied from those in accumulators and intermediates. These findings provide insight into Si isotope fractionation dynamics during uptake and translocation.
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Data availability
All data generated or analysed during this study are included in this published article.
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References
Barnes I, Moore L, Machlan L, Murphy T, Shields W (1975) Absolute isotopic abundance ratios and atomic weight of a reference sample of silicon. J Res Nat Bur Stand A 79:727–735. https://doi.org/10.6028/jres.094.034
Basile-Doelsch I (2006) Si stable isotopes in the Earth’s surface: A review. J Geochem Explor 88:252–256. https://doi.org/10.1016/j.gexplo.2005.08.050
Bern CR, Brzezinski MA, Beucher C, Ziegler K, Chadwick OA (2010) Weathering, dust, and biocycling effects on soil silicon isotope ratios. Geochim Cosmochim Acta 74:876–889. https://doi.org/10.1016/j.gca.2009.10.046
Cardinal D, Alleman LY, De Jong J, Ziegler K, André L (2003) Isotopic composition of silicon measured by multicollector plasma source mass spectrometry in dry plasma mode. J Anal at Spectrom 18:213–218. https://doi.org/10.1039/B210109B
Conley DJ (2002) Terrestrial ecosystems and the global biogeochemical silica cycle. Global Biogeochem Cycles 16:68-1-68–8. https://doi.org/10.1029/2002gb001894
Cooke J, DeGabriel JL, Hartley SE (2016) The functional ecology of plant silicon: geoscience to genes. Funct Ecol 30:1270–1276. https://doi.org/10.1111/1365-2435.12711
Cornelis JT, Delvaux B, Cardinal D, André L, Ranger J, Opfergelt S (2010a) Tracing mechanisms controlling the release of dissolved silicon in forest soil solutions using Si isotopes and Ge/Si ratios. Geochim Cosmochim Acta 74:3913–3924. https://doi.org/10.1016/j.gca.2010.04.056
Cornelis JT, Delvaux B, Titeux H (2010b) Contrasting silicon uptakes by coniferous trees: a hydroponic experiment on young seedlings. Plant Soil 336:99–106. https://doi.org/10.1007/s11104-010-0451-x
Cornelis JT, Delvaux B, Georg RB, Lucas Y, Ranger J, Opfergelt S (2011) Tracing the origin of dissolved silicon transferred from various soil-plant systems towards rivers: a review. Biogeosciences 8:89–112. https://doi.org/10.5194/bg-8-89-2011
Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Belanger RR (2019) The controversies of silicon’s role in plant biology. New Phytol 221:67–85. https://doi.org/10.1111/nph.15343
Delstanche S, Opfergelt S, Cardinal D, Elsass F, André L, Delvaux B (2009) Silicon isotopic fractionation during adsorption of aqueous monosilicic acid onto iron oxide. Geochim Cosmochim Acta 73:923–934. https://doi.org/10.1016/j.gca.2008.11.014
Ding TP, Tian SH, Sun L, Wu LH, Zhou JX, Chen ZY (2008a) Silicon isotope fractionation between rice plants and nutrient solution and its significance to the study of the silicon cycle. Geochim Cosmochim Acta 72:5600–5615. https://doi.org/10.1016/j.gca.2008.09.006
Ding TP, Zhou JX, Wan DF, Chen ZY, Wang CY, Zhang F (2008b) Silicon isotope fractionation in bamboo and its significance to the biogeochemical cycle of silicon. Geochim Cosmochim Acta 72:1381–1395. https://doi.org/10.1016/j.gca.2008.01.008
Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664. https://doi.org/10.1073/pnas.91.1.11
Frick DA, Remus R, Sommer M, Augustin J, Kaczorek D, von Blanckenburg F (2020) Silicon uptake and isotope fractionation dynamics by crop species. Biogeosciences 17:6475–6490. https://doi.org/10.5194/bg-17-6475-2020
Geilert S, Vroon PZ, Roerdink DL, Van Cappellen P, van Bergen MJ (2014) Silicon isotope fractionation during abiotic silica precipitation at low temperatures: Inferences from flow-through experiments. Geochim Cosmochim Acta 142:95–114. https://doi.org/10.1016/j.gca.2014.07.003
Guelke M, Von Blanckenburg F (2007) Fractionation of stable iron isotopes in higher plants. Environ Sci Technol 41:1896–1901. https://doi.org/10.1021/es062288j
Guntzer F, Keller C, Meunier JD (2011) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32:201–213. https://doi.org/10.1007/s13593-011-0039-8
Haynes RJ (2014) A contemporary overview of silicon availability in agricultural soils. J Plant Nutr Soil Sci 177:831–844. https://doi.org/10.1002/jpln.201400202
Henriet C, Bodarwe L, Dorel M, Draye X, Delvaux B (2008) Leaf silicon content in banana (Musa spp.) reveals the weathering stage of volcanic ash soils in Guadeloupe. Plant Soil 313:71–82. https://doi.org/10.1007/s11104-008-9680-7
Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic Variation in the Silicon Composition of Plants. Ann Bot 96:1027–1046. https://doi.org/10.1093/aob/mci255
Homberg A, Obst M, Knorr KH, Kalbitz K, Schaller J (2020) Increased silicon concentration in fen peat leads to a release of iron and phosphate and changes in the composition of dissolved organic matter. Geoderma 374. https://doi.org/10.1016/j.geoderma.2020.114422
Imtiaz M, Rizwan MS, Mushtaq MA, Ashraf M, Shahzad SM, Yousaf B, Saeed DA, Rizwan M, Nawaz MA, Mehmood S, Tu S (2016) Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: A review. C&a Carnes Aliment 183:521–529. https://doi.org/10.1016/j.jenvman.2016.09.009
Liang YC, Si J, Romheld 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 YC, Hua H, Yong-Guan Z, Jie Z, Chunmei C, Volker RM (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
Liu M, Xu M, Zhang X, Zhou J, Ma Q, Wu L (2021) Poorly crystalline Fe(II) mineral phases induced by nano zero-valent iron are responsible for Cd stabilization with different soil moisture conditions and soil types. Ecotoxicol Environ Saf 223:112616. https://doi.org/10.1016/j.ecoenv.2021.112616
Ma JF, Nishimura K, Takahashi E (1989) Effect of silicon on the growth of rice plant at different growth stages. Soil Sci Plant Nutr 35:347–356. https://doi.org/10.1080/00380768.1989.10434768
Ma JF, Miyake Y, Takahashi E (2001) Chapter 2 Silicon as a beneficial element for crop plants. Silicon in Agriculture 8:17–39. https://doi.org/10.1016/S0928-3420(01)80006-9
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 (2015) A cooperative system of silicon transport in plants. Trends Plant Sci 20:435–442. https://doi.org/10.1016/j.tplants.2015.04.007
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
Ma QX, Wen Y, Wang D, Sun X, Hill PW, Macdonald A, Chadwick DR, Wu LH, Jones DL (2020) Farmyard manure applications stimulate soil carbon and nitrogen cycling by boosting microbial biomass rather than changing its community composition. Soil Biol Biochem 144:107760. https://doi.org/10.1016/j.soilbio.2020.107760
Matichenkov VV, Bocharnikova EA (2001) Chapter 13 The relationship between silicon and soil physical and chemical properties. In: LE Datnoff, GH Snyder, GH Korndörfer (eds) Studies in Plant Science. Elsevier. https://doi.org/10.1016/S0928-3420(01)80017-3
Mitani N, Chiba Y, Yamaji N, Ma JF (2009) Identification and characterization of maize and barley Lsi2-like silicon efflux transporters reveals a distinct silicon uptake system from that in rice. Plant Cell 21:2133–2142. https://doi.org/10.1105/tpc.109.067884
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
Opfergelt S, Cardinal D, Henriet C, Draye X, André L, Delvaux B (2006) Silicon Isotopic Fractionation by Banana (Musa spp.) Grown in a Continuous Nutrient Flow Device. Plant Soil 285:333–345. https://doi.org/10.1007/s11104-006-9019-1
Opfergelt S, de Bournonville G, Cardinal D, André L, Delstanche S, Delvaux B (2009) Impact of soil weathering degree on silicon isotopic fractionation during adsorption onto iron oxides in basaltic ash soils, Cameroon. Geochim Cosmochim Acta 73:7226–7240. https://doi.org/10.1016/j.gca.2009.09.003
Opfergelt S, Delmelle P (2012) Silicon isotopes and continental weathering processes: Assessing controls on Si transfer to the ocean. CR Geosci 344:723–738. https://doi.org/10.1016/j.crte.2012.09.006
Opfergelt S, Delvaux B, André L, Cardinal D (2008) Plant silicon isotopic signature might reflect soil weathering degree. Biogeochemistry 91:163–175. https://doi.org/10.1007/s10533-008-9278-4
Riotte J, Sandhya K, Prakash NB, Audry S, Zambardi T, Chmeleff J, Buvaneshwari S, Meunier JD (2018) Origin of silica in rice plants and contribution of diatom Earth fertilization: insights from isotopic Si mass balance in a paddy field. Plant Soil 423:481–501. https://doi.org/10.1007/s11104-017-3535-z
Schaller J, Faucherre S, Joss H, Obst M, Goeckede M, Planer-Friedrich B, Peiffer S, Gilfedder B, Elberling B (2019) Silicon increases the phosphorus availability of Arctic soils. Sci Rep 9. https://doi.org/10.1038/s41598-018-37104-6.
Schaller J, Frei S, Rohn L, Gilfedder BS (2020) Amorphous Silica Controls Water Storage Capacity and Phosphorus Mobility in Soils. Front Environ Sci 8. https://doi.org/10.3389/fenvs.2020.00094
Schaller J, Puppe D, Kaczorek D, Ellerbrock R, Sommer M (2021) Silicon Cycling in Soils Revisited. Plants-Basel 10. https://doi.org/10.3390/plants10020295
Sun Y, Wu L, Li X, Sun L, Gao J, Ding T (2016) Silicon isotope fractionation in rice and cucumber plants over a life cycle: Laboratory studies at different external silicon concentrations. J Geophys Res Biogeosci 121:2829–2841. https://doi.org/10.1007/s11104-008-9552-1
Sun H, Duan Y, Mitani-Ueno N, Che J, Jia J, Liu J, Guo J, Ma JF, Gong H (2020) Tomato roots have a functional silicon influx transporter but not a functional silicon efflux transporter. Plant Cell Environ 43:732–744. https://doi.org/10.1111/pce.13679
Sun H, Duan Y, Qi X, Zhang L, Huo H, Gong H (2018) Isolation and functional characterization of CsLsi2, a cucumber silicon efflux transporter gene. Ann Bot 122:641–648. https://doi.org/10.1093/aob/mcy103
Sun L, Wu L, Ding T, Tian S (2008) Silicon isotope fractionation in rice plants, an experimental study on rice growth under hydroponic conditions. Plant Soil 304:291–300. https://doi.org/10.1007/s11104-008-9552-1
Sun Y, Wu L, Li X, Sun L, Gao J, Ding T, Zhu Y (2017) Silicon Isotope Fractionation in Maize and its Biogeochemical Significance. Anal Lett 50:2475–2490. https://doi.org/10.1080/00032719.2017.1295460
Sutton JN, André L, Cardinal D, Conley DJ, De Souza GF, Dean J, Dodd J, Ehlert C, Ellwood MJ, Frings PJ (2018) A review of the stable isotope bio-geochemistry of the global silicon cycle and its associated trace elements. Front Earth Sci 5:112. https://doi.org/10.3389/feart.2017.00112
Van Bockhaven J, De Vleesschauwer D, Hofte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J Exp Bot 64:1281–1293. https://doi.org/10.1093/jxb/ers329
Van den Boorn SH, Vroon PZ, van Belle CC, van der Wagt B, Schwieters J, van Bergen MJ (2006) Determination of silicon isotope ratios in silicate materials by high-resolution MC-ICP-MS using a sodium hydroxide sample digestion method. J Anal at Spectrom 21:734–742. https://doi.org/10.1039/B600933F
Wan D, Li Y, Song H (1997) Preparation of silicon isotopic standard materials. Ac Geosci Sinica 18:330–335
Wang W, Wei HZ, Jiang SY, Eastoe CJ, Guo Q, Lin YB (2016) Adsorption Behavior of Metasilicate on N-Methyl d-Glucamine Functional Groups and Associated Silicon Isotope Fractionation. Langmuir 32:8872–8881. https://doi.org/10.1021/acs.langmuir.6b02388
Yan GC, Nikolic M, Ye MJ, Xiao ZX, Liang YC (2018) Silicon acquisition and accumulation in plant and its significance for agriculture. J Integr Agric 17:2138–2150. https://doi.org/10.1016/S2095-3119(18)62037-4
Yang JL, Zhang GL (2019) Si cycling and isotope fractionation: Implications on weathering and soil formation processes in a typical subtropical area. Geoderma 337:479–490. https://doi.org/10.1016/j.geoderma.2018.09.047
Yang X, Song Z, Yu C, Ding F (2020) Quantification of different silicon fractions in broadleaf and conifer forests of northern China and consequent implications for biogeochemical Si cycling. Geoderma 361:114036. https://doi.org/10.1016/j.geoderma.2019.114036
Zhou J, Sun Y, Xiao H, Ma Q, Si L, Ni L, Wu L (2021a) Silicon uptake and translocation in low-silica rice mutants investigated by isotope fractionation. Agron J. https://doi.org/10.1002/agj2.20597
Zhou J, Si L, Xiao H, Sun Y, Ma Q, Liu M, Xu M, Wang J, Ni L, Wu L (2021b) Silicon isotope fractionation with a low-silica rice mutant reflects plant uptake strategy in response to different Si supply levels. Agron J. https://doi.org/10.1002/agj2.20937
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This research was funded by National Natural Science Foundation of China (31572194); National Youth Natural Science Foundation of China (31801936); the Science and Technology Project of Ningbo (202002N3106).
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Data curation, JJZ; funding acquisition, LHW; methodology, JJZ, ST, WKP, HX, YS, MX and MJL; writing—original draft, JJZ; writing—review and editing, QXM and LHW. All authors read and approved the final manuscript.
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Zhou, J., Tang, S., Pan, W. et al. Silicon isotope fractionation dynamics during uptake and translocation by various crop species under three soil types. Plant Soil 477, 41–55 (2022). https://doi.org/10.1007/s11104-021-05264-6
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DOI: https://doi.org/10.1007/s11104-021-05264-6