The superior properties of silver nanoparticles (AgNPs) has resulted in their broad utilization worldwide, but also the risk of irreversible environment infestation. The plant cuticle and cell wall can trap a large part of the nanoparticles and thus protect the internal cell structures, where the cytoskeleton, for example, reacts very quickly to the threat, and defense signaling is subsequently triggered. We therefore used not only wild-type Arabidopsis seedlings, but also the glabra 1 mutant, which has a different composition of the cuticle. Both lines had GFP-labeled microtubules (MTs), allowing us to observe their arrangement. To quantify MT dynamics, we developed a new microscopic method based on the FRAP technique. The number and growth rate of MTs decreased significantly after AgNPs, similarly in both lines. However, the layer above the plasma membrane thickened significantly in wild-type plants. The levels of three major stress phytohormone derivatives-jasmonic, abscisic, and salicylic acids-after AgNP (with concomitant Ag+) treatment increased significantly (particularly in mutant plants) and to some extent resembled the plant response after mechanical stress. The profile of phytohormones helped us to estimate the mechanism of response to AgNPs and also to understand the broader physiological context of the observed changes in MT structure and dynamics.

Deparment of Analytical Chemistry University of Chemistry and Technology Prague Technická 3 166 28 Prague Czech Republic

Department of Biochemistry and Microbiology University of Chemistry and Technology Prague Technická 3 166 28 Prague Czech Republic

Department of Solid State Engineering University of Chemistry and Technology Prague Technická 3 166 28 Prague Czech Republic

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences and Faculty of Science of Palacký University Šlechtitelů 27 78371 Olomouc Czech Republic

Zobrazit více v PubMed

Falsini S., Clemente I., Papini A., Tani C., Schiff S., Salvatici M.C., Petruccelli R., Benelli C., Giordano C., Gonnelli C., et al. When Sustainable Nanochemistry Meets Agriculture: Lignin Nanocapsules for Bioactive Compound Delivery to Plantlets. ACS Sustain. Chem. Eng. 2019;7:19935–19942. doi: 10.1021/acssuschemeng.9b05462. DOI

Siddiqui M.H., Al-whaibi M.H., Mohammad F. Nanotechnology and Plant Sciences. Springer; Berlin/Heidelberg, Germany: 2015.

Rastogi A., Zivcak M., Sytar O., Kalaji H.M., He X., Mbarki S., Brestic M. Impact of Metal and Metal Oxide Nanoparticles on Plant: A Critical Review. Front. Chem. 2017;8:7. doi: 10.3389/fchem.2017.00078. PubMed DOI PMC

Yan A., Chen Z. Impacts of Silver Nanoparticles on Plants: A Focus on the Phytotoxicity and Underlying Mechanism. Int. J. Mol. Sci. 2019;20:1003. doi: 10.3390/ijms20051003. PubMed DOI PMC

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

Geisler-Lee J., Wang Q., Yao Y., Zhang W., Geisler M., Li K., Huang Y., Chen Y., Kolmakov A., Ma X. Phytotoxicity, Accumulation and Transport of Silver Nanoparticles by Arabidopsis Thaliana. Nanotoxicology. 2012;7:323–337. doi: 10.3109/17435390.2012.658094. PubMed DOI

Kaegi R., Sinnet B., Zuleeg S., Hagendorfer H., Mueller E., Vonbank R., Boller M., Burkhardt M. Release of Silver Nanoparticles from Outdoor Facades. Environ. Pollut. 2010;158:2900–2905. doi: 10.1016/j.envpol.2010.06.009. PubMed DOI

Tripathi D.K., Tripathi A., Shweta, Singh S., Singh Y., Vishwakarma K., Yadav G., Sharma S., Singh V.K., Mishra R.K., et al. Uptake, Accumulation and Toxicity of Silver Nanoparticle in Autotrophic Plants, and Heterotrophic Microbes: A Concentric Review. Front. Microbiol. 2017;8:7. doi: 10.3389/fmicb.2017.00007. PubMed DOI PMC

Nawrath C., Schreiber L., Franke R.B., Geldner N., Reina-Pinto J.J., Kunst L. Apoplastic Diffusion Barriers in Arabidopsis. Arab. Book. 2013;11:e0167. doi: 10.1199/tab.0167. PubMed DOI PMC

Bao D., Oh Z.G., Chen Z. Characterization of Silver Nanoparticles Internalized by Arabidopsis Plants Using Single Particle ICP-MS Analysis. Front. Plant Sci. 2016;7:32. doi: 10.3389/fpls.2016.00032. PubMed DOI PMC

Larue C., Castillo-Michel H., Sobanska S., Cécillon L., Bureau S., Barthès V., Ouerdane L., Carrière M., Sarret G. Foliar Exposure of the Crop Lactuca Sativa to Silver Nanoparticles: Evidence for Internalization and Changes in Ag Speciation. J. Hazard. Mater. 2014;264:98–106. doi: 10.1016/j.jhazmat.2013.10.053. PubMed DOI

Schwab F., Zhai G., Kern M., Turner A., Schnoor J.L., Wiesner M.R. Barriers, Pathways and Processes for Uptake, Translocation and Accumulation of Nanomaterials in Plants—Critical Review. Nanotoxicology. 2016;10:257–278. doi: 10.3109/17435390.2015.1048326. PubMed DOI

Berhin A., de Belllis D., Franke R.B., Andrade Buono R., Nowack M., Nawrath C. The Root Cap Cuticle: A Cell Wall Structure for Seedling Establishment and Lateral Root Formation. Cell. 2019;176:1367–1378.e8. doi: 10.1016/j.cell.2019.01.005. PubMed DOI

Hegebarth D., Buschhaus C., Wu M., Bird D., Jetter R. The Composition of Surface Wax on Trichomes of Arabidopsis Thaliana Differs from Wax on Other Epidermal Cells. Plant J. 2016;88:762–774. doi: 10.1111/tpj.13294. PubMed DOI

Hegebarth D., Jetter R. Cuticular Waxes of Arabidopsis Thaliana Shoots: Cell-Type-Specific Composition and Biosynthesis. Plants. 2017;6:27. doi: 10.3390/plants6030027. PubMed DOI PMC

Xia Y., Yu K., Navarre D., Seebold K., Kachroo A., Kachroo P. The Glabra1 Mutation Affects Cuticle Formation and Plant Responses to Microbes. Plant Physiol. 2010;154:833–846. doi: 10.1104/pp.110.161646. PubMed DOI PMC

Pattanaik S., Patra B., Singh S.K., Yuan L. An Overview of the Gene Regulatory Network Controlling Trichome Development in the Model Plant, Arabidopsis. Front. Plant Sci. 2014;5:259. doi: 10.3389/fpls.2014.00259. PubMed DOI PMC

Perazza D., Herzog M., Hülskamp M., Brown S., Dorne A.-M., Bonneville J.-M. Trichome Cell Growth in Arabidopsis Thaliana Can Be Derepressed by Mutations in at Least Five Genes. Genetics. 1999;152:461–476. doi: 10.1093/genetics/152.1.461. PubMed DOI PMC

Marks M.D. Molecular Genetic Analysis of Trichome Development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997;48:137–163. doi: 10.1146/annurev.arplant.48.1.137. PubMed DOI

Liang S., Yang X., Deng M., Zhao J., Shao J., Qi Y., Liu X., Yu F., An L. A New Allele of the SPIKE1 Locus Reveals Distinct Regulation of Trichome and Pavement Cell Development and Plant Growth. Front. Plant Sci. 2019;10:16. doi: 10.3389/fpls.2019.00016. PubMed DOI PMC

Kim G.-T., Shoda K., Tsuge T., Cho K.-H., Uchimiya H., Yokoyama R., Nishitani K., Tsukaya H. The ANGUSTIFOLIA Gene of Arabidopsis, a Plant CtBP Gene, Regulates Leaf-Cell Expansion, the Arrangement of Cortical Microtubules in Leaf Cells and Expression of a Gene Involved in Cell-Wall Formation. EMBO J. 2002;21:1267–1279. doi: 10.1093/emboj/21.6.1267. PubMed DOI PMC

Lü B., Wang J., Zhang Y., Wang H., Liang J., Zhang J. AT14A Mediates the Cell Wall-Plasma Membrane-Cytoskeleton Continuum in Arabidopsis Thaliana Cells. J. Exp. Bot. 2012;63:4061–4069. doi: 10.1093/jxb/ers063. PubMed DOI PMC

Milewska-Hendel A., Zubko M., Stróż D., Kurczyńska E. Effect of Nanoparticles Surface Charge on the Arabidopsis Thaliana (L.) Roots Development and Their Movement into the Root Cells and Protoplasts. Int. J. Mol. Sci. 2019;20:1650. doi: 10.3390/ijms20071650. PubMed DOI PMC

Ma X., Geiser-Lee J., Deng Y., Kolmakov A. Interactions between Engineered Nanoparticles (ENPs) and Plants: Phytotoxicity, Uptake and Accumulation. Sci. Total Environ. 2010;408:3053–3061. doi: 10.1016/j.scitotenv.2010.03.031. PubMed DOI

Bücker-Neto L., Paiva A.L.S., Machado R.D., Arenhart R.A., Margis-Pinheiro M. Interactions between Plant Hormones and Heavy Metals Responses. Genet. Mol. Biol. 2017;40:373–386. doi: 10.1590/1678-4685-gmb-2016-0087. PubMed DOI PMC

Ogawa T., Ara T., Aoki K., Suzuki H., Shibata D. Transient Increase in Salicylic Acid and Its Glucose Conjugates after Wounding in Arabidopsis Leaves. Plant Biotechnol. 2010;27:205–209. doi: 10.5511/plantbiotechnology.27.205. DOI

Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. UHPLC–MS/MS Based Target Profiling of Stress-Induced Phytohormones. Phytochemistry. 2014;105:147–157. doi: 10.1016/j.phytochem.2014.05.015. PubMed DOI

Hu B., Deng F., Chen G., Chen X., Gao W., Long L., Xia J., Chen Z.-H. Evolution of Abscisic Acid Signaling for Stress Responses to Toxic Metals and Metalloids. Front. Plant Sci. 2020;11:909. doi: 10.3389/fpls.2020.00909. PubMed DOI PMC

Sanzari I., Leone A., Ambrosone A. Nanotechnology in Plant Science: To Make a Long Story Short. Front. Bioeng. Biotechnol. 2019;7:120. doi: 10.3389/fbioe.2019.00120. PubMed DOI PMC

Karami Mehrian S., de Lima R. Nanoparticles Cyto and Genotoxicity in Plants: Mechanisms and Abnormalities. Environ. Nanotechnol. Monit. Manag. 2016;6:184–193. doi: 10.1016/j.enmm.2016.08.003. DOI

Lv J., Christie P., Zhang S. Uptake, Translocation, and Transformation of Metal-Based Nanoparticles in Plants: Recent Advances and Methodological Challenges. Environ. Sci. Nano. 2019;6:41–59. doi: 10.1039/C8EN00645H. DOI

Kaveh R., Li Y.S., Ranjbar S., Tehrani R., Brueck C.L., Van Aken B. Changes in Arabidopsis Thaliana Gene Expression in Response to Silver Nanoparticles and Silver Ions. Environ. Sci. Technol. 2013;47:10637–10644. doi: 10.1021/es402209w. PubMed DOI

Chan J., Eder M., Crowell E.F., Hampson J., Calder G., Lloyd C. Microtubules and CESA Tracks at the Inner Epidermal Wall Align Independently of Those on the Outer Wall of Light-Grown Arabidopsis Hypocotyls. J. Cell Sci. 2011;124:1088–1094. doi: 10.1242/jcs.086702. PubMed DOI

Geitmann A., Nebenfãhr A. Navigating the Plant Cell: Intracellular Transport Logistics in the Green Kingdom. Mol. Biol. Cell. 2015;26:3373–3378. doi: 10.1091/mbc.E14-10-1482. PubMed DOI PMC

Dixit R., Cyr R. The Cortical Microtubule Array: From Dynamics to Organization. Plant Cell. 2004;16:2546–2552. doi: 10.1105/tpc.104.161030. PubMed DOI PMC

Cai G. Assembly and Disassembly of Plant Microtubules: Tubulin Modifications and Binding to MAPs. J. Exp. Bot. 2010;61:623–626. doi: 10.1093/jxb/erp395. PubMed DOI

Ma H., Liu M. The Microtubule Cytoskeleton Acts as a Sensor for Stress Response Signaling in Plants. Mol. Biol. Rep. 2019;46:5603–5608. doi: 10.1007/s11033-019-04872-x. PubMed DOI

Nick P. Microtubules, Signalling and Abiotic Stress. Plant J. 2013;75:309–323. doi: 10.1111/tpj.12102. PubMed DOI

Hardham A.R. Microtubules and Biotic Interactions. Plant J. 2013;75:278–289. doi: 10.1111/tpj.12171. PubMed DOI

Zhou S., Chen Q., Li X., Li Y. MAP65-1 Is Required for the Depolymerization and Reorganization of Cortical Microtubules in the Response to Salt Stress in Arabidopsis. Plant Sci. 2017;264:112–121. doi: 10.1016/j.plantsci.2017.09.004. PubMed DOI

Thion L., Mazars C., Nacry P., Bouchez D., Moreau M., Ranjeva R., Thuleau P. Plasma Membrane Depolarization-Activated Calcium Channels, Stimulated by Microtubule-Depolymerizing Drugs in Wild-Type Arabidopsis Thaliana Protoplasts, Display Constitutively Large Activities and a Longer Half-Life in Ton 2 Mutant Cells Affected in the organization of cortical microtubules. Plant J. 1998;13:603–610. doi: 10.1046/j.1365-313X.1998.00062.x. PubMed DOI

Krasylenko Y.A., Yemets A.I., Blume Y.B. Plant Microtubules Reorganization under the Indirect UV-B Exposure and during UV-B-Induced Programmed Cell Death. Plant Signal. Behav. 2013;8:e24031. doi: 10.4161/psb.24031. PubMed DOI PMC

Jacques E., Verbelen J.P., Vissenberg K. Mechanical Stress in Arabidopsis Leaves Orients Microtubules in a “continuous” Supracellular Pattern. BMC Plant Biol. 2013;13:1–7. doi: 10.1186/1471-2229-13-163. PubMed DOI PMC

Liu X., Yang Q., Wang Y., Wang L., Fu Y., Wang X. Brassinosteroids Regulate Pavement Cell Growth by Mediating BIN2-Induced Microtubule Stabilization. J. Exp. Bot. 2018;69:1037–1049. doi: 10.1093/jxb/erx467. PubMed DOI PMC

Ursache R., Andersen T.G., Marhavý P., Geldner N. A Protocol for Combining Fluorescent Proteins with Histological Stains for Diverse Cell Wall Components. Plant J. 2018;93:399–412. doi: 10.1111/tpj.13784. PubMed DOI

Bhamidi S., Shi L., Chatterjee D., Belisle J.T., Crick D.C., McNeil M.R. A Bioanalytical Method to Determine the Cell Wall Composition of Mycobacterium Tuberculosis Grown in Vivo. Anal. Biochem. 2012;421:240–249. doi: 10.1016/j.ab.2011.10.046. PubMed DOI

Buda G.J., Isaacson T., Matas A.J., Paolillo D.J., Rose J.K.C. Three-Dimensional Imaging of Plant Cuticle Architecture Using Confocal Scanning Laser Microscopy. Plant J. 2009;60:378–385. doi: 10.1111/j.1365-313X.2009.03960.x. PubMed DOI

Mayumi K., Shibaoka H. The Cyclic Reorientation of Cortical Microtubules on Walls with a Crossed Polylamellate Structure: Effects of Plant Hormones and an Inhibitor of Protein Kinases on the Progression of the Cycle. Protoplasma. 1996;195:112–122. doi: 10.1007/BF01279190. DOI

Marc J., Granger C.L., Brincat J., Fisher D.D., Kao T.H., McCubbin A.G., Cyr R.J. A GFP-MAP4 Reporter Gene for Visualizing Cortical Microtubule Rearrangements in Living Epidermal Cells. Plant Cell. 1998;10:1927–1939. doi: 10.1105/tpc.10.11.1927. PubMed DOI PMC

Sambade A., Pratap A., Buschmann H., Morris R.J., Lloyd C. The Influence of Light on Microtubule Dynamics and Alignment in the Arabidopsis Hypocotyl. Plant Cell. 2012;24:192–201. doi: 10.1105/tpc.111.093849. PubMed DOI PMC

Ehrhardt D.W., Shaw S.L. Microtubule Dynamics and Organization in the Plant Cortical Array. Annu. Rev. Plant Biol. 2006;57:859–875. doi: 10.1146/annurev.arplant.57.032905.105329. PubMed DOI

Medford J.I., Behringer F.J., Callos J.D., Feldmann K.A. Normal and Abnormal Development in the Arabidopsis Vegetative Shoot Apex. Plant Cell. 1992;4:631–643. doi: 10.2307/3869522. PubMed DOI PMC

Maes L., Inzé D., Goossens A. Functional Specialization of the TRANSPARENT TESTA GLABRA1 Network Allows Differential Hormonal Control of Laminal and Marginal Trichome Initiation in Arabidopsis Rosette Leaves. Plant Physiol. 2008;148:1453–1464. doi: 10.1104/pp.108.125385. PubMed DOI PMC

Noir S., Bömer M., Takahashi N., Ishida T., Tsui T.L., Balbi V., Shanahan H., Sugimoto K., Devoto A. Jasmonate Controls Leaf Growth by Repressing Cell Proliferation and the Onset of Endoreduplication While Maintaining a Potential Stand-by Mode. Plant Physiol. 2013;161:1930–1951. doi: 10.1104/pp.113.214908. PubMed DOI PMC

De Vleesschauwer D., Seifi H.S., Filipe O., Haeck A., Huu S.N., Demeestere K., Höfte M. The DELLA Protein SLR1 Integrates and Amplifies Salicylic Acid- and Jasmonic Acid-Dependent Innate Immunity in Rice. Plant Physiol. 2016;170:1831–1847. doi: 10.1104/pp.15.01515. PubMed DOI PMC

Denness L., McKenna J.F., Segonzac C., Wormit A., Madhou P., Bennett M., Mansfield J., Zipfel C., Hamann T. Cell Wall Damage-Induced Lignin Biosynthesis Is Regulated by a Reactive Oxygen Species- and Jasmonic Acid-Dependent Process in Arabidopsis. Plant Physiol. 2011;156:1364–1374. doi: 10.1104/pp.111.175737. PubMed DOI PMC

Ruan J., Zhou Y., Zhou M., Yan J., Khurshid M., Weng W., Cheng J., Zhang K. Jasmonic Acid Signaling Pathway in Plants. Int. J. Mol. Sci. 2019;20:2479. doi: 10.3390/ijms20102479. PubMed DOI PMC

Blume Y.B., Krasylenko Y.A., Yemets A.I. Mechanism of Plant Hormone Signaling under Stress. John Wiley & Sons, Inc.; Hoboken, NJ, USA: 2017. The Role of the Plant Cytoskeleton in Phytohormone Signaling under Abiotic and Biotic Stresses; pp. 127–185.

Nakamura M. Microtubule Nucleating and Severing Enzymes for Modifying Microtubule Array Organization and Cell Morphogenesis in Response to Environmental Cues. New Phytol. 2015;205:1022–1027. doi: 10.1111/nph.12932. PubMed DOI

Tulin A., McClerklin S., Huang Y., Dixit R. Single-Molecule Analysis of the Microtubule Cross-Linking Protein MAP65-1 Reveals a Molecular Mechanism for Contact-Angle-Dependent Microtubule Bundling. Biophys. J. 2012;102:802–809. doi: 10.1016/j.bpj.2012.01.008. PubMed DOI PMC

Luptovčiak I., Komis G., Takáč T., Ovečka M., Šamaj J. Katanin: A Sword Cutting Microtubules for Cellular, Developmental, and Physiological Purposes. Front. Plant Sci. 2017;8:1982. doi: 10.3389/fpls.2017.01982. PubMed DOI PMC

McNally F.J., Okawa K., Iwamatsu A., Vale R.D. Katanin, the Microtubule-Severing ATPase, Is Concentrated at Centrosomes. J. Cell Sci. 1996;109:561–567. doi: 10.1242/jcs.109.3.561. PubMed DOI

Elliott A., Shaw S.L. Update: Plant Cortical Microtubule Arrays. Plant Physiol. 2018;176:94–105. doi: 10.1104/pp.17.01329. PubMed DOI PMC

Lang I., Sassmann S., Schmidt B., Komis G. Plasmolysis: Loss of Turgor and Beyond. Plants. 2014;3:583–593. doi: 10.3390/plants3040583. PubMed DOI PMC

Nakano R.T., Yamada K., Bednarek P., Nishimura M., Hara-Nishimura I. ER Bodies in Plants of the Brassicales Order: Biogenesis and Association with Innate Immunity. Front. Plant Sci. 2014;5:73. doi: 10.3389/fpls.2014.00073. PubMed DOI PMC

Yamada K., Hara-Nishimura I., Nishimura M. Unique Defense Strategy by the Endoplasmic Reticulum Body in Plants. Plant Cell Physiol. 2011;52:2039–2049. doi: 10.1093/pcp/pcr156. PubMed DOI

Nakazaki A., Yamada K., Kunieda T., Sugiyama R., Hirai M.Y., Tamura K., Hara-Nishimura I., Shimada T. Leaf Endoplasmic Reticulum Bodies Identified in Arabidopsis Rosette Leaves Are Involved in Defense against Herbivory. Plant Physiol. 2019;179:1515–1524. doi: 10.1104/pp.18.00984. PubMed DOI PMC

Beyer E.M. A Potent Inhibitor of Ethylene Action in Plants. Plant Physiol. 1976;58:268–271. doi: 10.1104/pp.58.3.268. PubMed DOI PMC

Plett J.M., Mathur J., Regan S. Ethylene Receptor ETR2 Controls Trichome Branching by Regulating Microtubule Assembly in Arabidopsis Thaliana. J. Exp. Bot. 2009;60:3923–3933. doi: 10.1093/jxb/erp228. PubMed DOI PMC

Choudhury D., Xavier P.L., Chaudhari K., John R., Dasgupta A.K., Pradeep T., Chakrabarti G. Unprecedented Inhibition of Tubulin Polymerization Directed by Gold Nanoparticles Inducing Cell Cycle Arrest and Apoptosis. Nanoscale. 2013;5:4476–4489. doi: 10.1039/c3nr33891f. PubMed DOI

Wen Y., Geitner N.K., Chen R., Ding F., Chen P., Andorfer R.E., Govindan P.N., Ke P.C. Binding of Cytoskeletal Proteins with Silver Nanoparticles. RSC Adv. 2013;3:22002. doi: 10.1039/c3ra43281e. DOI

Li S., Lei L., Somerville C.R., Gu Y. Cellulose Synthase Interactive Protein 1 (CSI1) Links Microtubules and Cellulose Synthase Complexes. Proc. Natl. Acad. Sci. USA. 2012;109:185–190. doi: 10.1073/pnas.1118560109. PubMed DOI PMC

Mirabet V., Krupinski P., Hamant O., Meyerowitz E.M., Jönsson H., Boudaoud A. The Self-Organization of Plant Microtubules inside the Cell Volume Yields Their Cortical Localization, Stable Alignment, and Sensitivity to External Cues. PLoS Comput. Biol. 2018;14:e1006011. doi: 10.1371/journal.pcbi.1006011. PubMed DOI PMC

Ganguly A., Zhu C., Chen W., Dixit R. FRA1 Kinesin Modulates the Lateral Stability of Cortical Microtubules through Cellulose Synthase–Microtubule Uncoupling Proteins. Plant Cell. 2020;32:2508–2524. doi: 10.1105/tpc.19.00700. PubMed DOI PMC

Tian J., Han L., Feng Z., Wang G., Liu W., Ma Y., Yu Y., Kong Z. Orchestration of Microtubules and the Actin Cytoskeleton in Trichome Cell Shape Determination by a Plant-Unique Kinesin. eLife. 2015;4:e09351. doi: 10.7554/eLife.09351. PubMed DOI PMC

Seung D., Webster M.W., Wang R., Andreeva Z., Marc J. Dissecting the Mechanism of Abscisic Acid-Induced Dynamic Microtubule Reorientation Using Live Cell Imaging. Funct. Plant Biol. 2013;40:224. doi: 10.1071/FP12248. PubMed DOI

Sakiyama-Sogo M., Shibaoka H. Gibberellin A3 and Abscisic Acid Cause the Reorientation of Cortical Microtubules in Epicotyl Cells of the Decapitated Dwarf Pea. Plant Cell Physiol. 1993;34:431–437. doi: 10.1093/oxfordjournals.pcp.a078437. DOI

Lü B., Chen F., Gong Z.H., Xie H., Zhang J.H., Liang J.S. Intracellular Localization of Integrin-like Protein and Its Roles in Osmotic Stress-Induced Abscisic Acid Biosynthesis in Zea Mays. Protoplasma. 2007;232:35–43. doi: 10.1007/s00709-007-0278-3. PubMed DOI

De Torres Zabala M., Bennett M.H., Truman W.H., Grant M.R. Antagonism between Salicylic and Abscisic Acid Reflects Early Host-Pathogen Conflict and Moulds Plant Defence Responses. Plant J. 2009;59:375–386. doi: 10.1111/j.1365-313X.2009.03875.x. PubMed DOI

Li H., Xia H., Ding W., Li Y., Shi Q., Wang D., Tao X. Synthesis of Monodisperse, Quasi-Spherical Silver Nanoparticles with Sizes Defined by the Nature of Silver Precursors. Langmuir. 2014;30:2498–2504. doi: 10.1021/la4047148. PubMed DOI

Ambrose J.C., Cyr R. The Kinesin ATK5 Functions in Early Spindle Assembly in Arabidopsis. Plant Cell. 2007;19:226–236. doi: 10.1105/tpc.106.047613. PubMed DOI PMC

Ueda K., Matsuyama T., Hashimoto T. Visualization of Microtubules in Living Cells of TransgenicArabidopsis Thaliana. Protoplasma. 1999;206:201–206. doi: 10.1007/BF01279267. DOI

Murashige T., Skoog F. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant. 1962;15:473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x. DOI