Tubulin Acetylation Mediates Bisphenol A Effects on the Microtubule Arrays of Allium cepa and Triticum turgidum

Abstract

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 α-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.

The mechanism of root growth inhibition by the endocrine disruptor bisphenol A (BPA)

“…Based on these findings, our results suggest that BPA reduces meristem size and thus root length by inhibiting cell division through accumulating auxin in the meristem. However, it is also possible that BPA directly inhibits cell division since BPA disrupts microtubule arrays in Pisum sativa, the gymnosperm Abies cephalonica, Triticum turgidum (durum wheat), and Allium cepa (onion) (Adamakis et al, 2019(Adamakis et al, , 2016(Adamakis et al, , 2013.…”

“…Higher concentrations of BPA (over 30 µM) inhibited plant growth by enhancing reactive oxygen species and lipid peroxidation in Arabidopsis (Ali et al, 2017) and soybean (Zhang et al, 2016). It was also reported that approximately 50-100 ppm BPA disrupted microtubule arrays, thereby inhibiting cell division in pea (Pisum sativum L.), the gymnosperm Abies cephalonica, Triticum turgidum (durum wheat) and Allium cepa (onion) (Adamakis et al, 2019(Adamakis et al, , 2016(Adamakis et al, , 2013. In addition, 5-10 ppm BPA inhibited pollen tube growth by decreasing the deposition of cell wall components through disrupting Ca 2+ gradients and actin filaments in Picea meyeri (Chang et al, 2015).…”

Hydrogen Peroxide Production by the Spot-Like Mode Action of Bisphenol A

“…Detached leaves of A. thaliana maintained in Petri dishes on filter paper soaked with distilled water were considered as controls. Four to five leaves per experiment were treated with aqueous 50 and 100 mg L −1 (0.2 and 0.4 mM) BPA solutions, prepared from a stock solution of 200 mg L −1 at 21.5°C, pH 7.0 ( Staples et al., 1998 ; Adamakis et al., 2013 ; Adamakis et al., 2019 ), soaked on filter paper in Petri dishes, for 6, 12 and 24 h. Each treatment has been done in triplicate.…”

“…Although plants can absorb and metabolize BPA, at the same time BPA could deteriorate their cellular/physiological status ( Zhang et al., 2017 ). It has been shown that experimentally applied concentrations of BPA (mg/L) negatively affected the growth of many important crops, e.g., soybean ( Qui et al., 2013 ; Zhang et al., 2016 ; Jiao et al., 2017 ; Li X. et al., 2018 ; Zhang et al., 2018 ; Xiao et al., 2019 ), pea ( Adamakis et al., 2013 ), wheat ( Adamakis et al., 2019 ), maize ( Stavropoulou et al., 2018 ), rice ( Ali et al., 2016 ), cucumber ( Li Y. T. et al., 2018 ) and onion ( Adamakis et al., 2019 ); also of non-cultivated plants such as the Cephalonian fir ( Adamakis et al., 2016 ) and the model plant Arabidopsis thaliana ( Pan et al., 2013 ; Tian et al., 2014 ; Frejd et al., 2016 ; Ali et al., 2017 ; Rapala et al., 2017 ; Bahmani et al., 2020 ). Growth reduction effects have interestingly been found to occur also after environmentally relevant concentrations (μg/L) applied on cultivated crops, e.g., cabbage and tomato ( Staples et al., 2010 ), native plants such as oat ( Staples et al., 2010 ) and seagrasses ( Adamakis et al., 2018 ; Malea et al., 2020 ).…”

“…BPA-derived growth defects have been linked to either cytoskeletal derangement ( Adamakis et al., 2013 ; Adamakis et al., 2016 ; Adamakis et al., 2018 ; Stavropoulou et al., 2018 ; Adamakis et al., 2019 ), hormonal imbalance ( Frejd et al., 2016 ; Li X. et al., 2018 ; Bahmani et al., 2020 ), deterioration of the photosynthetic machinery ( Jiao et al., 2017 ; Kim et al., 2018 ; Li Y. T. et al., 2018 ) or ROS production ( Wang et al., 2015 ; Ali et al., 2016 ; Zhang et al., 2018 ; Xiao et al., 2019 ). It could therefore be concluded that BPA effects in plants are pleiotropic ( Xiao et al., 2020 ).…”