title: A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells.
abstract: Silicon (Si) alleviates cadmium (Cd) toxicity in rice (Oryza sativa). However, the chemical mechanisms at the single-cell level are poorly understood. Here, a suspension of rice cells exposed to Cd and/or Si treatments was investigated using a combination of plant cell nutritional, molecular biological, and physical techniques including in situ noninvasive microtest technology (NMT), polymerase chain reaction (PCR), inductively coupled plasma mass spectroscopy (ICP-MS), and atomic force microscopy (AFM) in Kelvin probe mode (KPFM). We found that Si-accumulating cells had a significantly reduced net Cd(2+) influx, compared with that in Si-limited cells. PCR analyses of the expression levels of Cd and Si transporters in rice cells showed that, when the Si concentration in the medium was increased, expression of the Si transporter gene Low silicon rice 1 (Lsi1) was up-regulated, whereas expression of the gene encoding the transporter involved in the transport of Cd, Natural resistance-associated macrophage protein 5 (Nramp5), was down-regulated. ICP-MS results revealed that 64% of the total Si in the cell walls was bound to hemicellulose constituents following the fractionation of the cell walls, and consequently inhibited Cd uptake. Furthermore, AFM in KPFM demonstrated that the heterogeneity of the wall surface potential was higher in cells cultured in the presence of Si than in those cultured in its absence, and was homogenized after the addition of Cd. These results suggest that a hemicellulose-bound form of Si with net negative charges is responsible for inhibition of Cd uptake in rice cells by a mechanism of [Si-hemicellulose matrix]Cd complexation and subsequent co-deposition.
authors: College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
authors: Jie
authors: J
authors: Ma
authors: College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
authors: Hongmei
authors: H
authors: Cai
authors: College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
authors: Congwu
authors: C
authors: He
authors: College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
authors: Wenjun
authors: W
authors: Zhang
authors: College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
authors: Lijun
authors: L
authors: Wang
mesh_terms: D001692:Biological Transport; D002104:Cadmium / Q000737:chemistry / Q000378:metabolism*; D027682:Cation Transport Proteins / Q000235:genetics / Q000378:metabolism; D002458:Cell Fractionation; D002473:Cell Wall / Q000737:chemistry / Q000378:metabolism / Q000502:physiology; D018506:Gene Expression Regulation, Plant; D013058:Mass Spectrometry; D018625:Microscopy, Atomic Force; D008855:Microscopy, Electron, Scanning; D012275:Oryza / Q000378:metabolism* / Q000648:ultrastructure; D059828:Plant Cells / Q000737:chemistry / Q000378:metabolism / Q000648:ultrastructure; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D011134:Polysaccharides / Q000737:chemistry* / Q000378:metabolism; D012825:Silicon / Q000737:chemistry* / Q000378:metabolism
chemical_list: D027682:Cation Transport Proteins; D010940:Plant Proteins; D011134:Polysaccharides; D002104:Cadmium; C007916:hemicellulose; D012825:Silicon
keywords: Si-Cd complexation; cadmium (Cd); cell wall; hemicellulose; rice (Oryza sativa); silicon (Si)
references: Casey WH, Kinrade SD, Knight CTG, Rains DW, Epstein E. 2004. Aqueous silicate complexes in wheat, Triticum aestivum L. Plant, Cell & Environment 27: 51-54.
references: Chakrabarti SK, James JC, Mirmira RG. 2002. Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic Transcription Factor, Pdx1: importance of chromatin structure in directing promoter binding. Journal of Biological Chemistry 277: 13286-13293.
references: Chen G, Liu Y, Wang R, Zhang J, Owens G. 2013. Cadmium adsorption by willow root: the role of cell walls and their subfractions. Environmental Science & Pollution Research 20: 5665-5672.
references: Chu CC, Wang CC, Sun CS, Hsu C, Yin KC, Chu CY, Bi FY. 1975. Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Scientia Sinica 18: 659-668.
references: Clemens S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719.
references: Cooke J, Leishman MR. 2011. Is plant ecology more siliceous than we realise? Trends in Plant Science 16: 61-68.
references: da Cunha KPV, do Nascimento CWA. 2009. Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water, Air, & Soil Pollution 197: 323-330.
references: Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC. 2001. Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environmental Toxicology & Chemistry 20: 2383-2396.
references: Duval JF, van Leeuwen HP. 2011. Rates of ionic reactions with charged nanoparticles in aqueous media. Journal of Physical Chemistry A 116: 6443-6451.
references: Epstein E. 2009. Silicon: its manifold roles in plants. Annals of Applied Biology 155: 155-160.
references: Fernández R, Fernández-Fuego D, Bertrand A, González A. 2014. Strategies for Cd accumulation in Dittrichia viscosa (L.) Greuter: role of the cell wall, non-protein thiols and organic acids. Plant Physiology & Biochemistry 78: 63-70.
references: Fry SC. 1986. Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annual Review of Plant Physiology 37: 165-186.
references: Fujihira M. 1999. Kelvin probe force microscopy of molecular surfaces. Annual Review of Materials Science 29: 353-380.
references: He C, Ma J, Wang LJ. 2015. A hemicellulose-bound form of silicon with potential to improve the mechanical properties and regeneration of the cell wall of rice. New Phytologist 206: 1051-1062.
references: He C, Wang LJ, Liu J, Liu X, Li X, Ma J, Lin Y, Xu F. 2013. Evidence for ‘silicon’ within the cell walls of suspension-cultured rice cells. New Phytologist 200: 700-709.
references: Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H. 2012. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proceedings of the National Academy of Sciences, USA 109: 19166-19171.
references: Kalis EJ, Davis TA, Town RM, Leeuwen HPV. 2009. Impact of ionic strength on Cd (II) partitioning between alginate gel and aqueous media. Environmental Science & Technology 43: 1091-1096.
references: Kaufman PB, Bigelow WC, Petering LB, Drogosz FB. 1969. Silica in developing epidermal cells of Avena internodes: electron microprobe analysis. Science 166: 1015-1017.
references: Kaufman PB, Dayanandan P, Franklin CI, Takeoka Y. 1985. Structure and function of silica bodies in the epidermal system of grass shoots. Annals of Botany 55: 487-507.
references: Kim YH, Khan AL, Kim DH, Lee SY, Kim KM, Waqas M, Jung HY, Shin JH, Kim JG, Lee IJ. 2014. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biology 14: 13.
references: Kinrade SD, Del Nin JW, Schach AS, Sloan TA, Wilson KL, Knight CT. 1999. Stable five-and six-coordinated silicate anions in aqueous solution. Science 285: 1542-1545.
references: Lavoie M, Campbell PG, Fortin C. 2012. Extending the biotic ligand model to account for positive and negative feedback interactions between cadmium and zinc in a freshwater alga. Environmental Science & Technology 46: 12129-12136.
references: Lavoie M, Campbell PG, Fortin C. 2014. Predicting cadmium accumulation and toxicity in a green alga in the presence of varying essential element concentrations using a biotic ligand model. Environmental Science & Technology 48: 1222-1229.
references: Liang Y, Sun W, Zhu YG, Christie P. 2007. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environmental Pollution 147: 422-428.
references: Liang Y, Wong JWC, Wei L. 2005. Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays) grown in cadmium contaminated soil. Chemosphere 58: 475-483.
references: Liu J, Li K, Xu J, Liang J, Lu X, Yang J, Zhu Q. 2003. Interaction of Cd and five mineral nutrients for uptake and accumulation in different rice cultivars and genotypes. Field Crops Research 83: 271-281.
references: Liu J, Ma J, He C, Li X, Zhang W, Xu F, Lin Y, Wang LJ. 2013. Inhibition of cadmium ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon. New Phytologist 200: 691-699.
references: Lü J, Delamarche E, Eng L, Bennewitz R, Meyer E, Güntherodt HJ. 1999. Kelvin probe force microscopy on surfaces: investigation of the surface potential of self-assembled monolayers on gold. Langmuir 15: 8184-8188.
references: Lu LL, Tian SK, Yang XE, Li TQ, He ZL. 2009. Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii. Journal of Plant Physiology 166: 579-587.
references: Lux A, Luxová M, Morita S, Abe J, Inanaga S. 1999. Endodermal silicification in developing seminal roots of lowland and upland cultivars of rice (Oryza sativa L.). Canadian Journal of Botany 77: 955-960.
references: Lux A, Martinka M, Vaculík M, White PJ. 2011. Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62: 21-37.
references: Ma JF. 2004. Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Science & Plant Nutrition 50: 11-18.
references: 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.
references: Maksimović JD, Mojović M, Maksimović V, Römheld V, Nikolic M. 2012. Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. Journal of Experimental Botany 63: 2411-2420.
references: Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J. 2010. Cadmium exposure in the population: from health risks to strategies of prevention. BioMetals 23: 769-782.
references: Neumann D, ZurNieden U. 2001. Silicon and heavy metal tolerance of higher plants. Phytochemistry 56: 685-692.
references: Nwugo CC, Huerta AJ. 2010. The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmium-stress. Journal of Proteome Research 10: 518-528.
references: Ohshima H, Kondo T. 1990. Relationship among the surface potential, Donnan potential and charge density of ion-penetrable membranes. Biophysical Chemistry 38: 117-122.
references: Palermo V, Palma M, Samorì P. 2006. Electronic characterization of organic thin films by Kelvin probe force microscopy. Advanced Materials 18: 145-164.
references: Prabagar S, Hodson MJ, Evans DE. 2011. Silicon amelioration of aluminium toxicity and cell death in suspension cultures of Norway spruce (Picea abies) Karst.). Environmental & Experimental Botany 70: 266-276.
references: Rodrigo-Moreno A, Andrés-Colás N, Poschenrieder C, Gunsé B, Peñarrubia L, Shabala S. 2013. Calcium- and potassium- permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant, Cell & Environment 36: 844-855.
references: Sanita di Toppi L, Gabbrielli R. 1999. Response to cadmium in higher plants. Environmental & Experimental Botany 41: 105-130.
references: Sasaki A, Yamaji N, Yokosho K, Ma JF. 2012. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24: 2155-2167.
references: Sebastian A, Prasad MNV. 2014. Cadmium minimization in rice. A review. Agronomy for Sustainable Development 34: 155-173.
references: Selvendran RR, O'Neill MA. 1987. Isolation and analysis of cell walls from plant material. Methods of Biochemical Analysis 32: 25-153.
references: Shi G, Cai Q, Liu C, Wu L. 2010. Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regulation 61: 45-52.
references: Shi XH, Zhang CC, Wang H, Zhang FS. 2005. Effect of Si on the distribution of Cd in rice seedlings. Plant and Soil 272: 53-60.
references: Shiraishi E, Inouhe M, Joho M, Tohoyama H. 2000. The cadmium-resistant gene, CAD2, which is a mutated putative copper-transporter gene (PCA1), controls the intracellular cadmium-level in the yeast S. cerevisiae. Current Genetics 37: 79-86.
references: Shomer I, Novacky AJ, Pike SM, Yermiyahu U, Kinraide TB. 2003. Electrical potentials of plant cell walls in response to the ionic environment. Plant Physiology 133: 411-422.
references: Sinensky AK, Belcher AM. 2007. Label-free and high-resolution protein/DNA nanoarray analysis using Kelvin probe force microscopy. Nature Nanotechnology 2: 653-659.
references: Tamai K, Ma JF. 2008. Reexamination of silicon effects on rice growth and production under field conditions using a low silicon mutant. Plant and Soil 307: 21-27.
references: Tanaka K, Fujimaki S, Fujiwara T, Yoneyama T, Hayashi H. 2007. Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.). Soil Science & Plant Nutrition 53: 72-77.
references: Thomas J, Darvill A, Albersheim P. 1989. Isolation and structural characterization of the pectic polysaccharide rhamnogalacturonan II from walls of suspension-cultured rice cells. Carbohydrate Research 185: 261-277.
references: Tsai CC, Chiang PL, Sun CJ, Lin TW, Tsai MH, Chang YC, Chen YT. 2011. Surface potential variations on a silicon nanowire transistor in biomolecular modification and detection. Nanotechnology 22: 135503.
references: Tsai CC, Hung HH, Liu CP, Chen YT, Pan CY. 2012. Changes in plasma membrane surface potential of PC12 cells as measured by Kelvin probe force microscopy. PLoS ONE 7: e33849.
references: Uraguchi S, Fujiwara T. 2013. Rice breaks ground for cadmium-free cereals. Current Opinion in Plant Biology 16: 328-334.
references: Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T. 2011. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proceedings of the National Academy of Sciences, USA 108: 20959-20964.
references: Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A. 2012. Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Annals of Botany 110: 433-443.
references: Verbruggen N, Hermans C, Schat H. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181: 759-776.
references: Wagner GJ. 1993. Accumulation of cadmium in crop plants and its consequences to human health. Advances in Agronomy 51: 173-212.
references: Wang P, Kinraide TB, Zhou D, Kopittke PM, Peijnenburg WJ. 2011. Plasma membrane surface potential: dual effects upon ion uptake and toxicity. Plant Physiology 155: 808-820.
references: Wang LJ, Wang Y, Chen Q, Cao W, Li M, Zhang F. 2000. Silicon induced cadmium tolerance of rice seedlings. Journal of Plant Nutrition 23: 1397-1406.
references: Weber M, Trampczynska A, Clemens S. 2006. Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant, Cell & Environment 29: 950-963.
references: Wu HL, Chen CL, Du J, Liu HF, Yan C, Zhang Y, He YJ, Wang YQ, Chu CC, Feng ZY et al. 2012. Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiology 158: 790-800.
references: Xiong J, An L, Lu H, Zhu C. 2009. Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230: 755-765.
references: Xu J, Sun J, Du L, Liu X. 2012. Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytologist 196: 110-124.
references: Yamaji N, Ma JF. 2011. Further characterization of a rice silicon efflux transporter, Lsi2. Soil Science & Plant Nutrition 57: 259-264.
references: Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ. 2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology 146: 602-611.
references: Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ. 2011. Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiology 155: 1885-1892.
references: Ye J, Yan C, Liu J, Lu H, Liu T, Song Z. 2012. Effects of silicon on the distribution of cadmium compartmentation in root tips of Kandelia obovata (Shene, Liu and Yong). Environmental Pollution 162: 369-373.
references: Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S et al. 2013. Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proceedings of the National Academy of Sciences, USA 110: E3631-E3639.
references: Zenk MH. 1996. Heavy metal detoxification in higher plants: a review. Gene 179: 21-30.
references: Zhang C, Wang L, Nie Q, Zhang W, Zhang F. 2008. Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environmental & Experimental Botany 62: 300-307.
references: Zhang Q, Yan C, Liu J, Lu H, Duan H, Du J, Wang W. 2014. Silicon alleviation of cadmium toxicity in mangrove (Avicennia marina) in relation to cadmium compartmentation. Journal of Plant Growth Regulation 33: 233-242.
references: Zhong H, Lauchli A. 1993. Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. Journal of Experimental Botany 44: 773-778.
references: Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ. 2012. Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta 236: 989-997.