{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T08:47:56Z","timestamp":1767862076576,"version":"3.49.0"},"reference-count":50,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2019,5,11]],"date-time":"2019-05-11T00:00:00Z","timestamp":1557532800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"State Scholarship Foundation of Greece (IKY)","award":["MIS 5001552"],"award-info":[{"award-number":["MIS 5001552"]}]},{"DOI":"10.13039\/501100002665","name":"Research Committee, Aristotle University of Thessaloniki","doi-asserted-by":"publisher","award":["89342"],"award-info":[{"award-number":["89342"]}],"id":[{"id":"10.13039\/501100002665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002665","name":"Research Committee, Aristotle University of Thessaloniki","doi-asserted-by":"publisher","award":["91913"],"award-info":[{"award-number":["91913"]}],"id":[{"id":"10.13039\/501100002665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>The effects of bisphenol A (BPA), a prevalent endocrine disruptor, on both interphase and mitotic microtubule array organization was examined by immunofluorescence microscopy in meristematic root cells of Triticum turgidum (durum wheat) and Allium cepa (onion). In interphase cells of A. cepa, BPA treatment resulted in substitution of cortical microtubules by annular\/spiral tubulin structures, while in T. turgidum BPA induced cortical microtubule fragmentation. Immunolocalization of acetylated \u03b1-tubulin revealed that cortical microtubules of T. turgidum were highly acetylated, unlike those of A. cepa. In addition, elevation of tubulin acetylation by trichostatin A in A. cepa resulted in microtubule disruption similar to that observed in T. turgidum. BPA also disrupted all mitotic microtubule arrays in both species. It is also worth noting that mitotic microtubule arrays were acetylated in both plants. As assessed by BPA removal, its effects are reversible. Furthermore, taxol-stabilized microtubules were resistant to BPA, while recovery from oryzalin treatment in BPA solution resulted in the formation of ring-like tubulin conformations. Overall, these findings indicate the following: (1) BPA affects plant mitosis\/cytokinesis by disrupting microtubule organization. (2) Microtubule disassembly probably results from impairment of free tubulin subunit polymerization. (3) The differences in cortical microtubule responses to BPA among the species studied are correlated to the degree of tubulin acetylation.<\/jats:p>","DOI":"10.3390\/biom9050185","type":"journal-article","created":{"date-parts":[[2019,5,13]],"date-time":"2019-05-13T05:35:39Z","timestamp":1557725739000},"page":"185","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Tubulin Acetylation Mediates Bisphenol A Effects on the Microtubule Arrays of Allium cepa and Triticum turgidum"],"prefix":"10.3390","volume":"9","author":[{"given":"Ioannis-Dimosthenis S.","family":"Adamakis","sequence":"first","affiliation":[{"name":"Department of Botany, Faculty of Biology, National and Kapodistrian University of Athens, 157 84 Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emmanuel","family":"Panteris","sequence":"additional","affiliation":[{"name":"Department of Botany, School of Biology, Aristotle University of Thessaloniki, 541 24 Thessaloniki, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eleftherios P.","family":"Eleftheriou","sequence":"additional","affiliation":[{"name":"Department of Botany, School of Biology, Aristotle University of Thessaloniki, 541 24 Thessaloniki, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,5,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"11899","DOI":"10.1073\/pnas.1502108112","article-title":"Threat of plastic pollution to seabirds is global, pervasive, and increasing","volume":"112","author":"Wilcox","year":"2015","journal-title":"PNAS"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1007\/s11270-014-2184-6","article-title":"The effects of plastic pollution on aquatic wildlife: Current situations and future solutions","volume":"225","author":"Sigler","year":"2014","journal-title":"Water Air Soil Pollut."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.coesh.2017.10.003","article-title":"Micro (nano) plastics: A threat to human health?","volume":"1","author":"Revel","year":"2018","journal-title":"Curr. Opin. Environ. Sci. Health"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.1016\/j.scitotenv.2011.04.038","article-title":"Environmental and health hazard ranking and assessment of plastic polymers based on chemical composition","volume":"409","author":"Lithner","year":"2011","journal-title":"Sci. Total Environ."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1016\/j.ecoenv.2009.02.005","article-title":"Acute and chronic toxicity testing of bisphenol A with aquatic invertebrates and plants","volume":"5","author":"Mihaich","year":"2009","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.jenvman.2012.03.021","article-title":"Bisphenol A exposure, effects, and policy: A wildlife perspective","volume":"104","author":"Flint","year":"2012","journal-title":"J. Environ. Manag."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.tox.2006.06.009","article-title":"Human exposure to bisphenol A","volume":"226","author":"Kang","year":"2006","journal-title":"Toxicology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.chroma.2006.10.037","article-title":"Simultaneous determination of the endocrine disrupting compounds nonylphenol, nonylphenol ethoxylates, triclosan and bisphenol A in wastewater and sewage sludge by gas chromatography\u2013mass spectrometry","volume":"1138","author":"Gatidou","year":"2007","journal-title":"J. Chromat. A"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1716","DOI":"10.1016\/j.chemosphere.2008.09.037","article-title":"Endocrine disrupting compounds in municipal and industrial wastewater treatment plants in Northern Greece","volume":"73","author":"Pothitou","year":"2008","journal-title":"Chemosphere"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1796","DOI":"10.1016\/j.watres.2007.11.003","article-title":"Occurrence and fate of endocrine disrupters in Greek sewage treatment plants","volume":"42","author":"Stasinakis","year":"2008","journal-title":"Water Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.toxlet.2007.11.001","article-title":"Bisphenol A is released from polycarbonate drinking bottles and mimics the neurotoxic actions of estrogen in developing cerebellar neurons","volume":"176","author":"Le","year":"2008","journal-title":"Toxicol. Lett."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1000","DOI":"10.1016\/j.chemosphere.2014.09.011","article-title":"Emission of bisphenol analogues including bisphenol A and bisphenol F from wastewater treatment plants in Korea","volume":"119","author":"Lee","year":"2015","journal-title":"Chemosphere"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/S1043-2760(98)00029-0","article-title":"Xenoestrogens: The emerging story of bisphenol A","volume":"9","author":"Steinmetz","year":"1998","journal-title":"Trends Endocrinol. Metabol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e26490","DOI":"10.4161\/endo.26490","article-title":"Low dose effects of bisphenol A: An integrated review of in vitro, laboratory animal, and epidemiology studies","volume":"1","author":"Vandenberg","year":"2013","journal-title":"Endocr. Disruptors"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.marenvres.2016.05.012","article-title":"Plastics and microplastics in the oceans: From emerging pollutants to emerged threat","volume":"128","author":"Avio","year":"2017","journal-title":"Marine Environ. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1111\/gcb.14020","article-title":"Microplastics as an emerging threat to terrestrial ecosystems","volume":"24","author":"Kloas","year":"2018","journal-title":"Glob. Chang. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1002\/(SICI)1097-0215(20000415)86:2<151::AID-IJC1>3.0.CO;2-0","article-title":"Mammalian cell transformation and aneuploidy induced by five bisphenols","volume":"86","author":"Tsutsui","year":"2000","journal-title":"Int. J. Cancer"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1016\/S0960-9822(03)00189-1","article-title":"Bisphenol A exposure causes meiotic aneuploidy in the female mouse","volume":"13","author":"Hunt","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1021\/cb700210u","article-title":"Bisphenol A directly targets tubulin to disrupt spindle organization in embryonic and somatic cells","volume":"3","author":"George","year":"2008","journal-title":"ACS Chem. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.tiv.2019.04.009","article-title":"Bisphenol A disrupts mitotic progression via disturbing spindle attachment to kinetochore and centriole duplication in cancer cell lines","volume":"59","author":"Kim","year":"2019","journal-title":"Toxicol. in Vitro"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.mrgentox.2012.10.012","article-title":"Effects of bisphenol A on the microtubule arrays in root meristematic cells of Pisum sativum L.","volume":"750","author":"Adamakis","year":"2013","journal-title":"Mutat. Res. Genet. Toxicol. Environ. Mutagen"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.chemosphere.2016.01.082","article-title":"Bisphenol A disrupts microtubules and induces multipolar spindles in dividing root tip cells of the gymnosperm Abies cephalonica","volume":"149","author":"Adamakis","year":"2016","journal-title":"Chemosphere"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.chemosphere.2017.12.099","article-title":"Disruption of actin filaments in Zea mays by bisphenol A depends on their crosstalk with microtubules","volume":"195","author":"Stavropoulou","year":"2018","journal-title":"Chemosphere"},{"key":"ref_24","first-page":"21","article-title":"Effects of estrogens on microtubule polymerization in vitro: Correlation with estrogenicity","volume":"103","author":"Metzler","year":"1995","journal-title":"Environ. Health Perspect."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1016\/j.cellsig.2010.10.014","article-title":"The ins and outs of tubulin acetylation: More than just a post-translational modification?","volume":"23","author":"Perdiz","year":"2011","journal-title":"Cell Signal"},{"key":"ref_26","first-page":"935","article-title":"Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol","volume":"35","author":"Baskin","year":"1994","journal-title":"Plant Cell Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1038\/sj.bjp.0707166","article-title":"HDAC inhibitors as anti-inflammatory agents","volume":"150","author":"Adcock","year":"2007","journal-title":"Br. J. Pharmacol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Shankar, S., and Srivastava, R.K. (2008). Histone deacetylase inhibitors: Mechanisms and clinical significance in cancer: HDAC inhibitor-induced apoptosis. Programmed Cell Death in Cancer Progression and Therapy, Springer.","DOI":"10.1007\/978-1-4020-6554-5_13"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2085","DOI":"10.1083\/jcb.101.6.2085","article-title":"Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms","volume":"101","author":"Piperno","year":"1985","journal-title":"J. Cell Biol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Eshun-Wilson, L., Zhang, R., Portran, D., Nachury, M., Toso, D., Lohr, T., Vendruscolo, M., Bonomi, M., James, F., and Nogales, E. (2019). Effects of \u03b1-tubulin acetylation on microtubule structure and stability. bioRxiv, 516591.","DOI":"10.1101\/516591"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1534","DOI":"10.1046\/j.1365-3040.1997.d01-44.x","article-title":"Heat stress affects the organization of microtubules and cell division in Nicotiana tabacum cells","volume":"20","author":"Smertenko","year":"1997","journal-title":"Plant Cell Environ."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1093\/pcp\/pcf028","article-title":"Aluminum-induced rapid changes in the microtubular cytoskeleton of tobacco cell lines","volume":"43","author":"Nick","year":"2002","journal-title":"Plant Cell Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1007\/s00299-009-0669-3","article-title":"Pb\/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L.","volume":"28","author":"Liu","year":"2009","journal-title":"Plant Cell Rep."},{"key":"ref_34","first-page":"59","article-title":"The cortical microtubules are a universal target of tungsten toxicity among land plant taxa","volume":"13","author":"Adamakis","year":"2010","journal-title":"J. Biol. Res. Thess."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"7590","DOI":"10.1007\/s11356-014-3880-x","article-title":"Aberration of mitosis by hexavalent chromium in some Fabaceae members is mediated by species-specific microtubule disruption","volume":"22","author":"Eleftheriou","year":"2015","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/j.ecoenv.2018.04.005","article-title":"The effects of Bisphenol A on the seagrass Cymodocea nodosa: Leaf elongation impairment and cytoskeleton disturbance","volume":"157","author":"Adamakis","year":"2018","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1007\/BF01282998","article-title":"Acetylated tubulin is found in all microtubule arrays of two species of pine","volume":"207","author":"Gilmer","year":"1999","journal-title":"Protoplasma"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1006\/cbir.1999.0520","article-title":"Cytoskeleton-induced alterations of the lectin activity in winter wheat under cold hardening and abscisic acid (ABA)","volume":"24","author":"Timofeeva","year":"2000","journal-title":"Cell Biol. Intern."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3531","DOI":"10.1242\/jcs.046813","article-title":"Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6","volume":"122","author":"Zilberman","year":"2009","journal-title":"J. Cell Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1038\/nchembio.2140","article-title":"Structural insights into HDAC6 tubulin deacetylation and its selective inhibition","volume":"12","author":"Miyake","year":"2016","journal-title":"Nat. Chem. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1111\/plb.12104","article-title":"Accumulation and post-translational modifications of plant tubulins","volume":"16","author":"Parrotta","year":"2014","journal-title":"Plant Biol."},{"key":"ref_42","first-page":"521","article-title":"Structural and functional features of lysine acetylation of plant and animal tubulins","volume":"16","author":"Rayevsky","year":"2017","journal-title":"Cell Biol. Intern."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1242\/jcs.92.1.57","article-title":"Microtubules are acetylated in domains that turn over slowly","volume":"92","author":"Webster","year":"1989","journal-title":"J. Cell Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1091\/mbc.e13-07-0387","article-title":"Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure","volume":"25","author":"Howes","year":"2014","journal-title":"Mol. Biol. Cell"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1126\/science.aai8764","article-title":"Microtubules acquire resistance from mechanical breakage through intralumenal acetylation","volume":"356","author":"Xu","year":"2017","journal-title":"Science"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1093\/jxb\/erp395","article-title":"Assembly and disassembly of plant microtubules: Tubulin modifications and binding to MAPs","volume":"61","author":"Cai","year":"2010","journal-title":"J. Exp. Bot."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1104\/pp.17.01329","article-title":"Update: Plant cortical microtubule arrays","volume":"176","author":"Elliott","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"238","DOI":"10.3389\/fpls.2019.00238","article-title":"Phosphorylation of plant Microtubule-Associated Proteins during cell division","volume":"10","author":"Samaj","year":"2019","journal-title":"Front Plant Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0163-7258(91)90078-Z","article-title":"The biochemistry of compounds with anti-microtubule activity in plant cells","volume":"51","author":"Morejohn","year":"1991","journal-title":"Pharmacol. Ther."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.cbi.2004.01.005","article-title":"Bisphenol A and its methylated congeners inhibit growth and interfere with microtubules in human fibroblasts in vitro","volume":"147","author":"Lehmann","year":"2004","journal-title":"Chem. Biol. Interact."}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/9\/5\/185\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:51:07Z","timestamp":1760187067000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/9\/5\/185"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5,11]]},"references-count":50,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2019,5]]}},"alternative-id":["biom9050185"],"URL":"https:\/\/doi.org\/10.3390\/biom9050185","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,5,11]]}}}