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Review

The biomineralization of silica induced stress tolerance in plants: a case study for aluminum toxicity

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Article: 2233179 | Received 11 Apr 2023, Accepted 06 Jun 2023, Published online: 11 Jul 2023

References

  • Han L, Che S. Anionic surfactant templated mesoporous silicas (AMSs). Chem Soc Rev. 2013;42(9):3740–7. doi:10.1039/C2CS35297D.
  • Wang LJ, Christine VP, Ruiz-Agudo E, Hövelmann J, Putnis A. In situ imaging of interfacial precipitation of phosphate on goethite. Environ Sci Technol Lett. 2015;49(7):4184–4192. doi:10.1021/acs.est.5b00312.
  • Feng YM, Li XW, Guo SX, Chen XY, Chen TX, He YM, Shabala S, Yu M. Extracellular silica nanocoat formed by layer-by-layer (LBL) self-assembly confers aluminum resistance in root border cells of pea (Pisum sativum). J Nanobiotechnology. 2019;17(1):53. doi:10.1186/s12951-019-0486-y.
  • Kochian LV. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol. 1995;46(1):237–260. doi:10.1146/annurev.pp.46.060195.001321.
  • Neumann D, Nieden UZ. Sllicon and heavy metal tolerance of higher plants. Phytochemistry. 2001;56(7):685–692. doi:10.1016/S0031-9422(00)00472-6.
  • Freitas LBD, Fernandes DM, Maia SCM, Fernanders M. Effects of silicon on aluminum toxicity in upland rice plants. Plant Soil. 2017;420(1–2):263–275. doi:10.1007/s11104-017-3397-4.
  • Hodson MJ, Evans DE, Dietz K-J. Aluminium–silicon interactions in higher plants: an update. J Exp Bot. 2020;71(21):6719–6729. doi:10.1093/jxb/eraa024.
  • Anala R, Nambisan P. Study of morphology and chemical composition of phytoliths on the surface of paddy straw. Paddy Water Environ. 2015;13(4):521–527. doi:10.1007/s10333-014-0468-5.
  • Kumar S, Natalio F, Elbaum R. Protein-driven biomineralization: Comparing silica formation in grass silica cells to other biomineralization processes. J Struct Biol. 2021;213(1):107665. doi:10.1016/j.jsb.2020.107665.
  • Bustillo MN, Talavera RR, Sanchiz B. Biomineralization and diagenesis in a miocene tadpole: a mineralogical and taphonomic study. J Iber Geol. 2019;45(4):609–624. doi:10.1007/s41513-019-00112-0.
  • Simkiss K. Biomineralization and detoxification. Calcif Tissue Res. 1977;24(2):199–200. doi:10.1007/BF02223316.
  • Kumar S, Milstein Y, Brami Y, Elbaum M, Elbaum R. Mechanism of silica deposition in sorghum silica cells. New Phytol. 2017;213(2):791–798. doi:10.1111/nph.14173.
  • Foo CWP, Huang J, Kaplan DL. Lessons from seashells: silica mineralization via protein templating. Trends Biotechnol. 2004;22(11):577–585. doi:10.1016/j.tibtech.2004.09.011.
  • Armbrust EV, Berges JA, Bowler C, Gree BR, Martinez D, Putnam N, Zhou S, Allen AE, Apt KE, Bechner M. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science. 2004;306(5693):79–86. doi:10.1126/science.1101156.
  • Sun XN, Yu XY, Cheng F, He W. Cationic polymeric template-mediated preparation of silica nanocomposites. Soft Matter. 2021;17(40):8995–9007. doi:10.1039/D1SM00773D.
  • Qiao S, Zeng GQ, Wang XT, Dai CG, Sheng MP, Chen Q, Xu F, Xu H. Multiple heavy metals immobilization based on microbially induced carbonate precipitation by ureolytic bacteria and the precipitation patterns exploration. Chemosphere. 2021;274:129661. doi:10.1016/j.chemosphere.2021.129661.
  • Feng Y, Kreslavski VD, Shmarev AN, Ivanov AA, Zharmukhamedov SK, Kosobryukhov A, Yu M, Allakhverdiev SI, Shabala S. Effects of iron oxide nanoparticles (Fe3O4) on growth, photosynthesis, antioxidant activity and distribution of mineral elements in wheat (Triticum aestivum) Plants. Plants. 2022;11(14):1894. doi:10.3390/plants11141894.
  • Wang YX, Stass A, Horst WJ. Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol. 2004;136(3):3762–3770. doi:10.1104/pp.104.045005.
  • Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V. Architecture and material properties of diatom shells provide effective mechanical protection. Nature. 2003;421(6925):841–843. doi:10.1038/nature01416.
  • Yao H, Dao M, Imholt T, Huang J, Wheele K, Bonilla A, Suresh S, Ortiz C. Protection mechanisms of the iron-plated armor of a deep-sea hydrothermal vent gastropod. Proc Natl Acad Sci USA. 2010;107(3):987–992. doi:10.1073/pnas.0912988107.
  • Romano P, Fabritius H, Raabe D. The exoskeleton of the lobster homarus americanus as an example of a smart anisotropic biological material. Acta Biomater. 2007;3(3):301–309. doi:10.1016/j.actbio.2006.10.003.
  • Huang SS, Liu RL, Sun ML, Li XF, Guan Y, Lian B. Transcriptome expression analysis of the gene regulation mechanism of bacterial mineralization tolerance to high concentrations of Cd2+. Sci Total Environ. 2022;806:150911. doi:10.1016/j.scitotenv.2021.150911.
  • Ikeda T. Bacterial biosilicification: A new insight into the global silicon cycle. Biosci Biotechnol Biochem. 2021;85(6):1324–1331. doi:10.1093/bbb/zbab069.
  • Kotzsch A, Groger P, Pawolski D, Bomans PHH, Sommerdijk NAJM, Schlierf M, Kroger N. Silicanin-1 is a conserved diatom membrane protein involved in silica biomineralization. BMC Biol. 2017;15(1):1–16. doi:10.1186/s12915-017-0400-8.
  • Kumar S, Adiram-Filiba N, Blum S, Sanchez-Lopez JA, Tzfadia O, Omid A, Volpin H, Heifetz Y, Goobes G, Elbaum R, et al. Siliplant1 protein precipitates silica in sorghum silica cells. J Exp Bot. 2020;71(21):6830–6843. doi:10.1093/jxb/eraa258.
  • Decher G. Fuzzy nanoassemblies: toward layered polymeric multicomposites. Science. 1997;277(5330):1232–1237. doi:10.1126/science.277.5330.1232.
  • Qhobosheane M, Santra S, Zhang P, Tan WH. Biochemically functionalized silica nano particles. Analyst (Lond). 2001;126(8):1274–1278. doi:10.1039/b101489g.
  • Galloway JM, Senior L, Fletcher JM, Beesley JL, Hodgson LR, Harniman RL, Mantell JM, Coombs J, Rhys GG, Xue WF, et al. Bioinspired silicification reveals structural detail in self-assembled peptide cages. Acs Nano. 2018;12(2):1420–1432. doi:10.1021/acsnano.7b07785.
  • Wang GC, Dr P, Wang LJ, Liu P, Yan Y, Xu XR, Tang RK. Extracellular silica nanocoat confers thermotolerance on individual cells: A case study of material-based fictionalization of living cells. Chembiochem. 2010;11(17):2368–2373. doi:10.1002/cbic.201000494.
  • Cui JJ, Liu HT. Mesoporous SiO2 produced by mineralization of yeast cells as an efficient electrocatalyst for oxygen reduction reaction. Russian Chem Bulletin. 2017;66(6):969–974. doi:10.1007/s11172-017-1840-6.
  • Çiğil AB, Urucu OA, Kahraman MV. Nanodiamond-containing polyethyleneimine hybrid materials for lead adsorption from aqueous media. J Appl Polym Sci. 2019;136(46):48241. doi:10.1002/app.48241.
  • Chang Y, Liu TT, Liu P, Meng LL, Li SJ, Guo YM, Yang L, Ma XM. Biomineralized nanosilica-based organelles endow living yeast cells with non-inherent biological functions. Chem Commun. 2020;56(42):5693–5696. doi:10.1039/D0CC02546A.
  • Zhang CX, Zhang XR, Zhao GH. Ferritin nanocage: a versatile nanocarrier utilized in the field of food, nutrition, and medicine. Nanomaterials. 2020;10(9):1894. doi:10.3390/nano10091894.
  • Ma J, Zhang X, Zhang W, Wang L. Multifunctionality of silicified nanoshells at cell interfaces of Oryza sativa. ACS Sust Chem & Eng. 2016;4(12):6792–6799. doi:10.1021/acssuschemeng.6b01736.
  • Ma J, Sheng HC, Li XL, Wang LJ. Itraq-based proteomic analysis reveals the mechanisms of silicon-mediated cadmium tolerance in rice (Oryza sativa) cells. Plant Physiol Bioch. 2016;104:71–80. doi:10.1016/j.plaphy.2016.03.024.
  • Feng YM, Chen XY, Li XW, Li YL, Nong W, Tang J, Han HX, Shi L, Shabala S, Yu M. Root border cells as a convenient single cell system to study plant-environmental interactions: A case study for aluminum tolerance. Front Soil Sci. 2022;2:909530. doi:10.3389/fsoil.2022.909530.
  • Feng Y, Li H, Zhang X, Li X, Zhang J, Shi L, Chen X, Nong W, Wang C, Shabala S, et al. Effects of cadmium stress on root and root border cells of some vegetable species with different types of root meristem. Life. 2022;12(9):1401. doi:10.3390/life12091401.
  • Delhaize E, Ryan PR. Aluminum toxicity and tolerance in plants. Plant Physiol. 1995;107(2):315–321. doi:10.1104/pp.107.2.315.
  • Clarkson DT. Interaction between aluminum and phosphorus on root surfaces and cell wall material. Plant Soil. 1967;27(3):347–356. doi:10.1007/BF01376328.
  • Ma JF, Sasaki M, Matsumoto H. Al-induced inhibition of root elongation in corn, zea mays L. is overcome by si addition. Plant Soil. 1997;188(2):171–176. doi:10.1023/A:1004274223516.
  • Hu YD, Li QY, Lee BD, Jun YS. Aluminum affects heterogeneous Fe (III) (hydr) oxide nucleation, growth, and ostwald ripening. Environ Sci Technol Lett. 2014;48(1):299–306. doi:10.1021/es403777w.
  • Schmohl N, Horst WJ. Cell wall pectin content modulates aluminum sensitivity of zea mays (L) cells grown in suspension culture. Plant, Cell Environ. 2000;23(7):735–742. doi:10.1046/j.1365-3040.2000.00591.x.
  • Schwarzerova K, Zelenková S, Nick P, Opatrný Z. Aluminum-induced rapid changes in the microtubular cytoskeleton of tobacco cell lines. Plant Cell Physiol. 2002;43(2):207. doi:10.1093/pcp/pcf028.
  • Zhu YZ, Liu DW, Liu ZY, Li YF. Impact of aluminum exposure on the immune system: a mini review. Environ Toxicol Pharmacol. 2012;35(1):82–87. doi:10.1016/j.etap.2012.11.009.
  • Huang WJ, Yang XD, Yao SC, LwinOo T, He HY, Wang AQ, Li CZ, He LF. Reactive oxygen species burst induced by aluminum stress triggers mitochondria-dependent programmed cell death in peanut root tip cells. Plant Physiol Bioch. 2014;82(3):76–84. doi:10.1016/j.plaphy.2014.03.037.
  • Taylor GJ, Mcdonald-Stephens JL, Hunter DB, Bertsch MP, Elmore D, Rengel Z, Reid RJ. Direct measurement of aluminum uptake and distribution in single cells of chara corallina. Plant Physiol. 2000;123(3):987–996. doi:10.1104/pp.123.3.987.
  • De Tombeur F, Vander LC, Cornelis JT, Godin B, Compere P, Delvaux B. Soil and climate affect foliar silicification patterns and silica-cellulose balance in sugarcane (Saccharum officinarum). Plant Soil. 2020;452(1–2):529–546. doi:10.1007/s11104-020-04588-z.
  • Pedersen O, Revsbech NP, Shabala S, Napier R. Microsensors in plant biology: In vivo visualization of inorganic analytes with high spatial and/or temporal resolution. J Exp Bot. 2020;71(14):3941–3954. doi:10.1093/jxb/eraa175.
  • Shabala S, Newman I. Salinity effects on the activity of plasma membrane H+ and Ca2+ transporters in bean leaf mesophyll: masking role of the cell wall. Ann Bot. 2000;85(5):681–686. doi:10.1006/anbo.2000.1131.
  • Shamayeva K, Spurna K, Kulik N, Kale D, Munko O, Spurny P, Zayats V, Ludwig J. Mpm motifs of the yeast skt protein trk1 can assemble to form a functional k+-translocation system. Biochimica et Biophysica Acta (BBA) - Biomembr. 2021;1863(2):183513. doi:10.1016/j.bbamem.2020.183513.
  • Fan C, Li Y, Hu Z, Hu H, Wang G, Li A, Wang Y, Tu Y, Xia T, Peng L, et al. Ectopic expression of a novel OsExtensin-like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice. Plant Biotechnol J. 2018;16(1):254–263. doi:10.1111/pbi.12766.
  • Yarbrough JM, Himmel ME, Ding SY. Plant cell wall characterization using scanning probe microscopy techniques. Biotechnol Biofuels. 2009;2(1):1–11. doi:10.1186/1754-6834-2-17.
  • Ding SY, Liu YS, Zeng Y, Himmel ME, Baker JO, Bayer EA. How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science. 2012;338(6110):1055–1060. doi:10.1126/science.1227491.
  • Zhang YN, Zhang MM, Reese RA, Zhang HQ, Xu BQ. Real-time single molecular study of a pretreated cellulose hydrolysis mode and individual enzyme movement. Biotechnol Biofuels. 2016;9(1):1–12. doi:10.1186/s13068-016-0498-x.
  • Dayo A, Gupta I, Dandina R. Nanoscale investigation of silicon dioxide nanofluids and implications for enhanced oil recovery – an atomic force microscope study. J Petrol Sci Eng. 2020;191:107165. doi:10.1016/j.petrol.2020.107165.
  • Fuchigami S, Niina T, Takada S. Biomolecular data assimilation to integrate high-speed atomic force microscopy measurement and molecular simulation-science direct. Biophys J. 2020;118(3):33. doi:10.1016/j.bpj.2019.11.360.
  • Galkin O, Vekilov PG. Direct determination of the nucleation rates of protein crystals. J Phys Chem B. 1999;103(49):10965–10971. doi:10.1021/jp992786x.
  • Wallace AF, DeYoreo JJ, Dove PM. Kinetics of silica nucleation on carboxyl-and amine-terminated surfaces: insights for biomineralization. J Am Chem Soc. 2009;131(14):5244–5250. doi:10.1021/ja809486b.
  • Neethirajan S, Gordon R, Wang LJ. Potential of silica bodies (phytoliths) for nanotechnology. Trends Biotechnol. 2009;27(8):461–467. doi:10.1016/j.tibtech.2009.05.002.
  • Nawaz MA, Zakharenko AM, Zemchenko IV, Haider MS, Ali MA, Imtiaz M, Chung G, Tsatsakis A, Sun S, Golokhvast KS. Phytolith formation in plants: from soil to cell. Plants. 2019;8(8):249. doi:10.3390/plants8080249.
  • Parry DW, Smithson F. Types of opaline silica depositions in the leaves of British grasses. Ann Bot. 1964;28(1):169–185. doi:10.1093/oxfordjournals.aob.a083891.
  • Guo ZM, Wang C, Wang LJ, Cao CS, Chen X, Sun CR, Li TJ. A new biological synthetic route for preparation of silica nanoparticles. Mol Cryst Liq Cry. 1999;337(1):249–252. doi:10.1080/10587259908023424.
  • Lawton JR. Observations on the structure of epidermal cells, particularly the cork and silica cells, from the flowering stem internode of Lolium temulentum L. (Gramineae). Bot J Linn Soc. 1980;80(2):161–177. doi:10.1111/j.1095-8339.1980.tb01663.x.
  • Simpson TL, Simpson TL, Volcani BE. Silicon and siliceous structure in biological systems. Vol. 216. New York: Springer; 1981. p. 1310. doi:10.1007/978-1-4612-5944-2
  • Berni R, Luyckx M, Xu X, Legay S, Sergeant K, Hausman JF, Lutts S, Cai G, Guerriero G. Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environ Exp Bot. 2019;161:98–106. doi:10.1016/j.envexpbot.2018.10.017.