Skip to main content
Log in

Distribution and Speciation of Cu in the Root Border Cells of Rice by STXM Combined with NEXAFS

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Root border cells (RBCs) serve plants in their initial line of defense against stress from the presence of heavy metals in the soil. In this research, light microscopy and synchrotron-based scanning transmission X-ray microscopy (STXM) combined with near edge X-ray absorption fine structure spectroscopy (NEXAFS) with a nanoscale spatial resolution were used to investigate the effects of copper (Cu) upon the RBCs, as well as its distribution and speciation within the RBCs of rice (Oryza sativa L.) under aeroponic culture. The results indicated that with increasing exposure time and concentration, the attached RBCs were surrounded by a thick mucilage layer which changed in form from an ellipse into a strip in response to Cu ion stress. Copper was present as Cu(II), which accumulated not only in the cell wall but also in the cytoplasm. To our knowledge, this is the first time that STXM has been used in combination with NEXAFS to provide new insight into the distribution and speciation of metal elements in isolated plant cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allan DL, Jarrell WM (1989) Proton and copper adsorption to maize and soybean root cell walls. Plant Physiol 89:823–832

    Article  CAS  Google Scholar 

  • Arrua RD, Hitchcock AP, Hon WB, West M, Hilder EF (2014) Characterization of polymer monoliths containing embedded nanoparticles by scanning transmission X-ray microscopy (STXM). Anal Chem 86:2876–2881

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  Google Scholar 

  • Barcelo J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92

    Article  CAS  Google Scholar 

  • Brigham LA, Woo HH, Hawes MC (1995) Root border cells as tools in plant cell studies. Method Cell Biol 49:377–387

    Article  CAS  Google Scholar 

  • Cai MZ, Wang FM, Li RF, Zhang SN, Wang N, Xu GD (2011a) Response and tolerance of root border cells to aluminum toxicity in soybean seedlings. J Inorg Biochem 105:966–971

    Article  CAS  Google Scholar 

  • Cai MZ, Zhang SN, Xing CH, Wang FM, Wang N, Zhu L (2011b) Developmental characteristics and aluminum resistance of root border cells in rice seedlings. Plant Sci 180:702–708

    Article  CAS  Google Scholar 

  • Cai M, Wang N, Xing C, Wang F, Wu K, Du X (2013) Immobilization of aluminum with mucilage secreted by root cap and root border cells is related to aluminum resistance in Glycine max L. Environ Sci Pollut Res 20:8924–8933

    Article  CAS  Google Scholar 

  • Chen WR, Liu P, Xu G, Cai MZ, Yu HN, Chen MY (2008) Effects of Al3+ on the biological characteristics of cowpea root border cells. Acta Physiol Plant 30:303–308

    Article  CAS  Google Scholar 

  • Cohen-Shoel N, Ilzycer D, Gilath I, Tel-Or E (2002) The involvement of pectin in Sr2+ biosorption by Azolla. Water Air Soil Pollut 135:195–205

    Article  CAS  Google Scholar 

  • Driouich A, Durand C, Vicre-Gibouin M (2007) Formation and separation of root border cells. Trends Plant Sci 12:14–19

    Article  CAS  Google Scholar 

  • Dynes JJ, Tyliszczak T, Araki T, Lawrence JR, Swerhone GDW, Leppard GG, Hitchcock AP (2006) Speciation and quantitative mapping of metal species in microbial biofilms using scanning transmission X-ray microscopy. Environ Sci Technol 40:1556–1565

    Article  CAS  Google Scholar 

  • Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ 28:1410–1420

    Article  CAS  Google Scholar 

  • Feldman LJ (1984) The development and dynamics of the root apical meristem. Am J Bot 71:1308–1314

    Article  CAS  Google Scholar 

  • Gunawardena U, Rodriguez M, Straney D, Romeo JT, VanEtten HD, Hawes MC (2005) Tissue-specific localization of pea root infection by Nectria haematococca. Mech Conseq Plant Physiol 137:1363–1374

    Article  CAS  Google Scholar 

  • Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Z (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327

    Article  CAS  Google Scholar 

  • Hawes MC, Gunawardena U, Miyasaka S, Zhao XW (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133

    Article  CAS  Google Scholar 

  • Hawes MC, Curlango-Rivera G, Xiong Z, Kessler JO (2012) Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’. Plant Soil 355:1–16

    Article  CAS  Google Scholar 

  • Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186:1520–1526

    Article  CAS  Google Scholar 

  • Jaroszuk-Scisel J, Kurek E, Rodzik B, Winiarczyk K (2009) Interactions between rye (Secale cereale) root border cells (RBCs) and pathogenic and nonpathogenic rhizosphere strains of Fusarium culmorum. Mycol Res 113:1053–1061

    Article  Google Scholar 

  • Jiang HD et al (2013) Three-dimensional coherent X-ray diffraction imaging of molten iron in mantle olivine at nanoscale resolution. Phys Rev Lett 110(205501):1–4

    Google Scholar 

  • Jouvin D et al (2012) Stable isotopes of Cu and Zn in higher plants: evidence for Cu reduction at the root surface and two conceptual models for isotopic fractionation processes. Environ Sci Technol 46:2652–2660

    Article  CAS  Google Scholar 

  • Lin H, Shi J, Wu B, Yang J, Chen Y, Zhao Y, Hu T (2010) Speciation and biochemical transformations of sulfur and copper in rice rhizosphere and bulk soil—XANES evidence of sulfur and copper associations. J Soil Sediment 10:907–914

    Article  CAS  Google Scholar 

  • Liu D, Kottke I (2004) Subcellular localization of copper in the root cells of Allium sativum by electron energy loss spectroscopy (EELS). Bioresour Technol 94:153–158

    Article  CAS  Google Scholar 

  • Liu T, Li F, Zhang X, Shi J, Chen Y (2012) The number and surviral rate of corn root border cells under the stress of copper ions. Plant Physiol J (Chin) 48:669–675

    Google Scholar 

  • Luo T, Tian HX, Guo Z, Zhuang GQ, Jing CY (2013) Fate of arsenate adsorbed on nano-TiO2 in the presence of sulfate reducing bacteria. Environ Sci Technol 47:10939–10946

    Article  CAS  Google Scholar 

  • Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987

    Article  CAS  Google Scholar 

  • Peng C et al (2011) Graphene-templated formation of two-dimensional lepidocrocite nanostructures for high-efficiency catalytic degradation of phenols. Energy Environ Sci 4:2035–2040

    Article  CAS  Google Scholar 

  • Pongrac P et al (2013) Spatially resolved distributions of the mineral elements in the grain of tartary buckwheat (Fagopyrum tataricum). Food Res Int 54:125–131

    Article  CAS  Google Scholar 

  • Regvar M, Eichert D, Kaulich B, Gianoncelli A, Pongrac P, Vogel-Mikus K (2013) Biochemical characterization of cell types within leaves of metal-hyperaccumulating Noccaea praecox (Brassicaceae). Plant Soil 373:157–171

    Article  CAS  Google Scholar 

  • Remusat L, Hatton PJ, Nico PS, Zeller B, Kleber M, Derrien D (2012) NanoSIMS study of organic matter associated with soil aggregates: advantages, limitations, and combination with STXM. Environ Sci Technol 46:3943–3949

    Article  CAS  Google Scholar 

  • Si J, Zhao H, Wang X, Yao C, Deng G, Feng K (2008) Effects of different copper levels on subcellular distribution and chemical forms of copper in maize cells. J Agro-Environ Sci 27:452–456

    CAS  Google Scholar 

  • Tamas L, Budikova S, Huttova J, Mistrik I, Simonovicova M, Siroka B (2005) Aluminum-induced cell death of barley-root border cells is correlated with peroxidase- and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Rep 24:189–194

    Article  CAS  Google Scholar 

  • Tolra R et al (2011) Localization of aluminium in tea (Camellia sinensis) leaves using low energy X-ray fluorescence spectro-microscopy. J Plant Res 124:165–172

    Article  CAS  Google Scholar 

  • Wang J, Hitchcock AP, Karunakaran C (2009) 3D chemical and elemental imaging of biological samples by STXM spectro-tomography. Act Rep 2009:154–155

    Google Scholar 

  • Wang Y, Huang J, Gao Y (2013) Subcellular accumulation of different concentrations of cadmium, nickel, and copper in Indian mustard and application of a sigmoidal model. J Environ Qual 42:1142–1150

    Article  CAS  Google Scholar 

  • Weigel HJ, Jäger HJ (1980) Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol 65:480–482

    Article  CAS  Google Scholar 

  • Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783

    Article  CAS  Google Scholar 

  • Wen F, White GJ, VanEtten HD, Xiong Z, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829

    Article  CAS  Google Scholar 

  • Xue C et al (2010) High-performance soft X-ray spectromicroscopy beamline at SSRF. Rev Sci Instrum 81:103502. doi:10.1063/1.3491837

    Article  Google Scholar 

  • Yi Z, Peng L, JinMin S, GenDi X, MiaoZhen C, TingTing W (2009) Morphological and physiological response of the root tip border cells to Fe2+ toxicity in rice. Plant Nutr Fertil Sci 15:763–770

    Google Scholar 

  • Zhang XZ et al (2010) Ratio-contrast imaging of dual-energy absorption for element mapping with a scanning transmission X-ray microscope. J Synchrotron Radiat 17:804–809

    Article  CAS  Google Scholar 

  • Zhang P et al (2012) Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano 6:9943–9950

    Article  CAS  Google Scholar 

  • Zhang LJ et al (2013) Imaging interfacial micro- and nano-bubbles by scanning transmission soft X-ray microscopy. J Synchrotron Radiat 20:413–418

    Article  CAS  Google Scholar 

  • Zhu M, Ahn SJ, Matsumoto H (2003) Inhibition of growth and development of root border cells in wheat by Al. Physiol Plant 117:359–367

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by the National Natural Science Foundation of China (21177109, 11179025, 41422107) and Program for New Century Excellent Talents in University (NCET-11-0455). We would like to express our gratitude to Xiangjun Zhen and Zhi Guo at beamline BL08U1A of the Shanghai Synchrotron Radiation Facility for their generous help in data collection and processing. We are also grateful to Chidong Zhou in Zhejiang University for his help in the art processing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jiyan Shi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peng, C., Wang, Y., Sun, L. et al. Distribution and Speciation of Cu in the Root Border Cells of Rice by STXM Combined with NEXAFS. Bull Environ Contam Toxicol 96, 408–414 (2016). https://doi.org/10.1007/s00128-015-1716-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-015-1716-0

Keywords

Navigation