Uptake of water and nutrients by roots affects the ontogenesis of the whole plant. Nanoparticles, e.g. gold nanoparticles, have a broad range of applications in many fields which leads to the transfer of these materials into the environment. Thus, the understanding of their impact on the growth and development of the root system is an emerging issue. During our studies on the effect of positively charged gold nanoparticles on the barley roots, a hairless phenotype was found. We investigated whether this phenotype correlates with changes in symplasmic communication, which is an important factor that regulates, among others, differentiation of the rhizodermis into hair and non-hair cells. The results showed no restriction in symplasmic communication in the treated roots, in contrast to the control roots, in which the trichoblasts and atrichoblasts were symplasmically isolated during their differentiation. Moreover, differences concerning the root morphology, histology, ultrastructure and the cell wall composition were detected between the control and the treated roots. These findings suggest that the harmful effect of nanoparticles on plant growth may, among others, consist in disrupting the symplasmic communication/isolation, which leads to the development of a hairless root phenotype, thus limiting the functioning of the roots.

Department of Cell Biology Faculty of Biology and Environmental Protection University of Silesia in Katowice 28 Jagiellońska Street 40 032 Katowice Poland

Department of Physics University of Hradec Králové Hradec Králové Czech Republic

Institute of Materials Science Faculty of Computer Science and Materials Science University of Silesia in Katowice 75 Pułku Piechoty Street 1a Chorzów 41 500 Poland

Institute of Plant Biology and Biotechnology Faculty of Biotechnology and Horticulture University of Agriculture in Krakow Al 29 Listopada 54 31 425 Krakow Poland

Laboratory of Microscopy Techniques Faculty of Biology and Environmental Protection University of Silesia in Katowice 28 Jagiellońska Street 40 032 Katowice Poland

See more in PubMed

Cox A, Venkatachalam P, Sahi S, Sharma N. Reprint of: silver and titanium dioxide nanoparticle toxicity in plants: a review of current research. Plant Physiol Biochem. 2017;110:33–49. doi: 10.1016/j.plaphy.2016.08.007. PubMed DOI

Milewska-Hendel, A., Gawecki, R., Zubko, M., Stróż, D. & Kurczyńska, E. Diverse influence of nanoparticles on plant growth with a particular emphasis on crop plants. Acta Agrobot69, 10.5586/aa.1694 (2016).

Tripathi DK, et al. An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol Biochem. 2017;110:2–12. doi: 10.1016/j.plaphy.2016.07.030. PubMed DOI

Cailloux M. Metabolism and absorption of water by root hairs. Can J Bot. 1972;50:557–573. doi: 10.1139/b72-069. DOI

Fohse D, Claassen N, Jungk A. Phosphorus efficiency of plants: II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in 7 plant-species. Plant Soil. 1991;132:261–272. doi: 10.1007/BF00010407. DOI

Itoh S, Barber SA. A numerical-solution of whole plant nutrient-uptake for soil-root systems with root hairs. Plant Soil. 1983;70:403–413. doi: 10.1007/BF02374895. DOI

Marzec M, Melzer M, Szarejko I. Asymmetric growth of root epidermal cells is related to the differentiation of root hair cells in Hordeum vulgare (L.) J Exp Bot. 2013;64:5145–5155. doi: 10.1093/jxb/ert300. PubMed DOI PMC

Bates TR, Lynch JP. The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot. 2000;87:964–970. doi: 10.2307/2656995. PubMed DOI

Cormack RGH. The development of root hairs by Elodea canadensis. New Phytol. 1937;36:19–25. doi: 10.1111/j.1469-8137.1937.tb06900.x. DOI

Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K. Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development. 1994;120:3247–3255.

Kim CM, Dolan L. Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. New Phytol. 2011;192:601–610. doi: 10.1111/j.1469-8137.2011.03839.x. PubMed DOI

Duhan JS, et al. Nanotechnology: the new perspective in precision agriculture. Biotechnol Rep. 2017;15:11–23. doi: 10.1016/j.btre.2017.03.002. PubMed DOI PMC

Kah, M. Nanopesticides and nanofertilizers: emerging contaminants or opportunities for risk mitigation? Front Chem3, 10.3389/fchem.2015.00064 (2015). PubMed PMC

Solanki, P., Bhargava, A., Chhipa, H., Jain, N. & Panwar, J. Nano-fertilizers and their smart delivery system in Nanotechnologies in food and agriculture (eds Rai, M., Ribeiro, C., Mattoso, L. & Duran, N.) 81–101 (Springer, 2015).

Subramanian, K. S., Manikandan, A., Thirunavukkarasu, M. & Rahale C.S. Nano-fertilizers for balanced crop nutrition in Nanotechnologies in food and agriculture (eds Rai, M., Ribeiro, C., Mattoso, L. & Duran, N.) 69–80 (Springer, 2015).

Oberdorster G, Oberdorster E, Oberdorster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 2005;113:823–839. doi: 10.1289/ehp.7339. PubMed DOI PMC

Yanık F, Vardar F. Toxic effects of aluminum oxide (Al2O3) nanoparticles on root growth and development in Triticum aestivum. Water Air Soil Pollut. 2015;226:296. doi: 10.1007/s11270-015-2566-4. DOI

Garcia-Sanchez, S., Bernales, I. & Cristobal, S. Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signalling. BMC Genomics16, 10.1186/s12864-015-1530-4 (2015). PubMed PMC

Nair PMG, Chung IM. Physiological and molecular level effects of silver nanoparticles exposure in rice (Oryza sativa L.) seedlings. Chemosphere. 2014;112:105–113. doi: 10.1016/j.chemosphere.2014.03.056. PubMed DOI

Benitez-Alfonso Y. Symplastic intercellular transport from a developmental perspective. J Exp Bot. 2014;65:1857–1863. doi: 10.1093/jxb/eru067. PubMed DOI

Brunkard JO, Runkel AM, Zambryski PC. Plasmodesmata dynamics are coordinated by intracellular signaling pathways. Curr Opin Plant Biol. 2013;16:614–620. doi: 10.1016/j.pbi.2013.07.007. PubMed DOI PMC

Dresselhaus T. Cell-cell communication during double fertilization. Curr Opin Plant Biol. 2006;9:41–47. doi: 10.1016/j.pbi.2005.11.002. PubMed DOI

Han Y-Z, Huang B-Q, Zee S-Y, Yuan M. Symplastic communication between the central cell and the egg apparatus cells in the embryo sac of Torenia fournieri Lind. before and during fertilization. Planta. 2000;211:158–162. doi: 10.1007/s004250000289. PubMed DOI

Kim I, Kobayashi K, Cho E, Zambryski PC. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. P Natl Acad Sci USA. 2005;102:11945–11950. doi: 10.1073/pnas.0505622102. PubMed DOI PMC

Kim I, Zambryski PC. Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis. Curr Opin Plant Biol. 2005;8:593–599. doi: 10.1016/j.pbi.2005.09.013. PubMed DOI

Marzec, M. & Kurczynska, E. Importance of symplasmic communication in cell differentiation. Plant Signal Behav9, 10.4161/psb.27931 (2014). PubMed PMC

Stadler R, Lauterbach C, Sauer N. Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 2005;139:701–712. doi: 10.1104/pp.105.065607. PubMed DOI PMC

Wrobel J, Barlow PW, Gorka K, Nabialkowska D, Kurczynska EU. Histology and symplasmic tracer distribution during development of barley androgenic embryos. Planta. 2011;233:873–881. doi: 10.1007/s00425-010-1345-0. PubMed DOI PMC

Wrobel-Marek J, Kurczynska E, Plachno BJ, Kozieradzka-Kiszkurno M. Identification of symplasmic domains in the embryo and seed of Sedum acre L. (Crassulaceae) Planta. 2017;245:491–505. doi: 10.1007/s00425-016-2619-y. PubMed DOI PMC

Maule, A. J., Gaudioso-Pedraza, R. & Benitez-Alfonso, Y. Callose deposition and symplastic connectivity are regulated prior to lateral root emergence. Commun Integr Biol6, 10.4161/cib.26531 (2013). PubMed PMC

Marzec M, Muszynska A, Melzer M, Sas-Nowosielska H, Kurczynska EU. Increased symplasmic permeability in barley root epidermal cells correlates with defects in root hair development. Plant Biology. 2014;16:476–484. doi: 10.1111/plb.12066. PubMed DOI PMC

Maule AJ, Benitez-Alfonso Y, Faulkner C. Plasmodesmata - membrane tunnels with attitude. Curr Opin Plant Biol. 2011;14:683–690. doi: 10.1016/j.pbi.2011.07.007. PubMed DOI

Otero S, Helariutta Y, Benitez-Alfonso Y. Symplastic communication in organ formation and tissue patterning. Curr Opin Plant Biol. 2016;29:21–28. doi: 10.1016/j.pbi.2015.10.007. PubMed DOI

Robards AW, Lucas WJ. Plasmodesmata. Annu Rev Plant Phys. 1990;41:369–419. doi: 10.1146/annurev.pp.41.060190.002101. DOI

Roberts AG, Oparka KJ. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 2003;26:103–124. doi: 10.1046/j.1365-3040.2003.00950.x. DOI

Zambryski P, Crawford K. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Bi. 2000;16:393–421. doi: 10.1146/annurev.cellbio.16.1.393. PubMed DOI

Bouyer D, et al. Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol. 2008;6:1166–1177. doi: 10.1371/journal.pbio.0060141. PubMed DOI PMC

Kurata T, et al. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development. 2005;132:5387–5398. doi: 10.1242/dev.02139. PubMed DOI

Tominaga R, et al. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development. 2008;135:1335–1345. doi: 10.1242/dev.017947. PubMed DOI

Horiunova II, Krasylenko YA, Yemets AI, Blume YB. Involvement of plant cytoskeleton in cellular mechanisms of metal toxicity. Cytol Genet. 2016;50:47–59. doi: 10.3103/S0095452716010060. PubMed DOI

Gahoonia TS, Nielsen NE. Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica. 1997;98:177–182. doi: 10.1023/A:1003113131989. DOI

Ma Z, Bielenberg DG, Brown KM, Lynch JP. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 2001;24:459–467. doi: 10.1046/j.1365-3040.2001.00695.x. DOI

Nair PMG, Chung IM. Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsis thaliana. Environ Sci Pollut R. 2014;21:8858–8869. doi: 10.1007/s11356-014-2822-y. PubMed DOI

Burch-Smith TM, Zambryski PC. Plasmodesmata paradigm shift: regulation from without versus within. Annu Rev Plant Biol. 2012;63:239–260. doi: 10.1146/annurev-arplant-042811-105453. PubMed DOI

Kragler F, Monzer J, Shash K, Xoconostle-Cazares B, Lucas WJ. Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J. 1998;15:367–381. doi: 10.1046/j.1365-313X.1998.00219.x. DOI

Benitez-Alfonso Y, et al. Symplastic intercellular connectivity regulates lateral root patterning. Develop Cell. 2013;26:136–147. doi: 10.1016/j.devcel.2013.06.010. PubMed DOI

Lucas WJ, Ham BK, Kim JY. Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol. 2009;19:495–503. doi: 10.1016/j.tcb.2009.07.003. PubMed DOI

Kang YH, Song SK, Schiefelbein J, Lee MM. Nuclear trapping controls the position-dependent localization of CAPRICE in the root epidermis of Arabidopsis. Plant Physiol. 2013;163:193–204. doi: 10.1104/pp.113.221028. PubMed DOI PMC

O’Lexy R, et al. Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose. J Exp Bot. 2018;69:3715–3728. doi: 10.1093/jxb/ery171. PubMed DOI PMC

Yin L, et al. More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol. 2011;45:2360–2367. doi: 10.1021/es103995x. PubMed DOI

Ding B, Parthasarathy MV, Niklas K, Turgeon R. A morphometric analysis of the phloem-unloading pathway in developing tobacco leaves. Planta. 1988;176:307–318. doi: 10.1007/BF00395411. PubMed DOI

Juniper BE, Barlow PW. The distribution of plasmodesmata in the root tip of maize. Planta. 1969;89:352–360. doi: 10.1007/BF00387235. PubMed DOI

Ma F, Peterson CA. Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways. J Exp Bot. 2001;52:1051–1061. doi: 10.1093/jexbot/52.358.1051. PubMed DOI

Robards AW, Jackson SM, Clarkson DT, Sanderson J. The structure of barley roots in relation to the transport of ions into the stele. Protoplasma. 1973;77:291–311. doi: 10.1007/BF01276765. DOI

Seagull RW. Differences in the frequency and disposition of plasmodesmata resulting from root cell elongation. Planta. 1983;159:497–504. doi: 10.1007/BF00409138. PubMed DOI

Zhu T, Rost TL. Directional cell-to-cell communication in the Arabidopsis root apical meristem III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination. Protoplasma. 2000;213:99–107. doi: 10.1007/BF01280510. DOI

Robards, A. W. & Clarkson, D. T. The role of plasmodesmata in the transport of water and nutrients across roots in Intercellular communication in plants: studies on plasmodesmata (eds Gunning, B. E. S. & Robards, A. W) 181–201 (Springer, 1976).

Karas I, McCully ME. Further studies of the histology of lateral root development in Zea mays. Protoplasma. 1973;77:243–269. doi: 10.1007/BF01276762. DOI

Vanbel AJE, Oparka KJ. On the validity of plasmodesmograms. Bot Acta. 1995;108:174–182. doi: 10.1111/j.1438-8677.1995.tb00849.x. DOI

Bell K, Oparka K. Imaging plasmodesmata. Protoplasma. 2011;248:9–25. doi: 10.1007/s00709-010-0233-6. PubMed DOI

Demchenko, K. N., Voitsekhovskaja, O. V. & Pawlowski, K. Plasmodesmata without callose and calreticulin in higher plants - open channels for fast symplastic transport? Front Plant Sci5, 10.3389/fpls.2014.00074 (2014). PubMed PMC

De Storme, N. & Geelen, D. Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front Plant Sci5, 10.3389/fpls.2014.00138 (2014). PubMed PMC

Schulz A. Plasmodesmal widening accompanies the short-term increase in symplasmic phloem unloading in pea root-tips under osmotic-stress. Protoplasma. 1995;188:22–37. doi: 10.1007/BF01276793. DOI

Blee KA, Anderson AJ. Regulation of arbuscule formation by carbon in the plant. Plant J. 1998;16:523–530. doi: 10.1046/j.1365-313x.1998.00315.x. DOI

van der Wel NN, Goldbach RW, van Lent JWM. The movement protein and coat protein of alfalfa mosaic virus accumulate in structurally modified plasmodesmata. Virology. 1998;244:322–329. doi: 10.1006/viro.1998.9117. PubMed DOI

Kim DW, et al. Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell. 2006;18:2958–2970. doi: 10.1105/tpc.106.045229. PubMed DOI PMC

Dolan L, Costa S. Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot. 2001;52:413–417. doi: 10.1093/jxb/52.suppl_1.413. PubMed DOI

Salazar-Henao JE, Schmidt W. An inventory of nutrient-responsive genes in Arabidopsis root hairs. Front Plant Sci. 2016;7:237. doi: 10.3389/fpls.2016.00237. PubMed DOI PMC

Marzec, M., Melzer, M. & Szarejko, I. The evolutionary context of root epidermis cell patterning in grasses (Poaceae) Plant Signal Behav9, 10.4161/psb.27972 (2015). PubMed PMC

Zidan I, Azaizeh H, Neumann PM. Does salinity reduce growth in maize root epidermal cells by inhibiting their capacity for cell wall acidification? Plant Physiol. 1990;93:7–11. doi: 10.1104/pp.93.1.7. PubMed DOI PMC

Dinneny JR, et al. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science. 2008;320:942–945. doi: 10.1126/science.1153795. PubMed DOI

Potocka I, Szymanowska-Pulka J. Morphological responses of plant roots to mechanical stress. Ann Bot. 2018;122:711–723. PubMed PMC

Ochoa-Villarreal, M., Aispuro-Hernández, E., Vargas-Arispuro, I. & Martínez-Téllez, M. Á. Plant cell wall polymers: function, structure and biological activity of their derivatives in Polymerization (ed. De Souza Gomes A.) 64–89 (InTech, 2012).

Potocka I, Godel K, Dobrowolska I, Kurczynska EU. Spatio-temporal localization of selected pectic and arabinogalactan protein epitopes and the ultrastructural characteristics of explant cells that accompany the changes in the cell fate during somatic embryogenesis in Arabidopsis thaliana. Plant Physiol Biochem. 2018;127:573–589. doi: 10.1016/j.plaphy.2018.04.032. PubMed DOI

Majewska-Sawka A, Nothnagel EA. The multiple roles of arabinogalactan proteins in plant development. Plant Physiol. 2000;122:3–10. doi: 10.1104/pp.122.1.3. PubMed DOI PMC

Sala K, Malarz K, Barlow PW, Kurczynska EU. Distribution of some pectic and arabinogalactan protein epitopes during Solanum lycopersicum (L.) adventitious root development. BMC Plant Biol. 2017;17:25. doi: 10.1186/s12870-016-0949-3. PubMed DOI PMC

Milewska-Hendel, A. et al. Quantitative and qualitative characteristics of cell wall components and prenyl lipids in the leaves of Tilia x euchlora trees growing under salt stress. PloS one12, 10.1371/journal.pone.0172682 (2017). PubMed PMC

Lamport, D. T. A., Tan, L., Held, M. & Kieliszewski, M. J. The role of the primary cell wall in plant morphogenesis. Int J Mol Sci19, 10.3390/ijms19092674 (2018). PubMed PMC

Daher FB, Braybrook SA. How to let go: pectin and plant cell adhesion. Front Plant Sci. 2015;6:523. doi: 10.3389/fpls.2015.00523. PubMed DOI PMC

Braybrook SA. Analyzing cell wall elasticity after hormone treatment: an example using tobacco BY-2 cells and auxin. Methods Mol Biol. 2017;1497:125–133. doi: 10.1007/978-1-4939-6469-7_12. PubMed DOI

Mustafa G, Komatsu S. Toxicity of heavy metals and metal-containing nanoparticles on plants. Biochim Biophys Acta. 2016;1864:932–944. doi: 10.1016/j.bbapap.2016.02.020. PubMed DOI

Muszynski A, et al. Xyloglucan, galactomannan, glucuronoxylan, and rhamnogalacturonan I do not have identical structures in soybean root and root hair cell walls. Planta. 2015;242:1123–1138. doi: 10.1007/s00425-015-2344-y. PubMed DOI

Pena MJ, Kong Y, York WS, O’Neill MA. A galacturonic acid-containing xyloglucan is involved in Arabidopsis root hair tip growth. Plant Cell. 2012;24:4511–4524. doi: 10.1105/tpc.112.103390. PubMed DOI PMC

Chen XY, Kim JY. Callose synthesis in higher plants. Plant Signal Behav. 2009;4:489–492. doi: 10.4161/psb.4.6.8359. PubMed DOI PMC

Chen MH, Citovsky V. Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J. 2003;35:386–392. doi: 10.1046/j.1365-313X.2003.01818.x. PubMed DOI

Brecknock S, et al. High resolution scanning electron microscopy of plasmodesmata. Planta. 2011;234:749–758. doi: 10.1007/s00425-011-1440-x. PubMed DOI

Knox JP, Benitez-Alfonso Y. Roles and regulation of plant cell walls surrounding plasmodesmata. Curr Opin Plant Biol. 2014;22:93–100. doi: 10.1016/j.pbi.2014.09.009. PubMed DOI

Milewska-Hendel A, Zubko M, Karcz J, Stroz D, Kurczynska E. Fate of neutral-charged gold nanoparticles in the roots of the Hordeum vulgare L. cultivar Karat. Sci Rep. 2017;7:3014. doi: 10.1038/s41598-017-02965-w. PubMed DOI PMC

Kirschner, G. K., Stahl, Y., Von Korff, M. & Simon, R. Unique and conserved features of the barley root meristem. Front Plant Sci8, 10.3389/fpls.2017.01240 (2017). PubMed PMC

Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC. Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development. 2002;129:1261–1272. PubMed

Betekhtin A, et al. Organ and tissue-specific localisation of selected cell wall epitopes in the zygotic embryo of Brachypodium distachyon. Int J Mol Sci. 2018;19:725. doi: 10.3390/ijms19030725. PubMed DOI PMC

Clausen MH, Willats WG, Knox JP. Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydr Res. 2003;338:1797–1800. doi: 10.1016/S0008-6215(03)00272-6. PubMed DOI

Jones L, Seymour GB, Knox JP. Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1[->]4)-[β]-D-galactan. Plant Physiol. 1997;113:1405–1412. doi: 10.1104/pp.113.4.1405. PubMed DOI PMC

Yates EA, et al. Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology. 1996;6:131–139. doi: 10.1093/glycob/6.2.131. PubMed DOI

Smallwood M, Yates EA, Willats WG, Martin H, Knox JP. Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta. 1996;198:452–459. doi: 10.1007/BF00620063. DOI

Pennell RI, et al. Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell. 1991;3:1317–1326. doi: 10.1105/tpc.3.12.1317. PubMed DOI PMC

Effect of Nanoparticles Surface Charge on the Arabidopsis thaliana (L.) Roots Development and Their Movement into the Root Cells and Protoplasts