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Ukr. Bot. J. 2020, 77(3): 225–231
Cell Biology and Molecular Biology

Involvement of cytoskeleton microtubules in the formation of induced aerenchyma in adventitious roots of Zea mays (Poaceae)

Shevchenko G.V.

Plants of Zea mays were grown for 12 days in sulfur-deficient medium according to a standard technique applied specifically for formation of aerenchyma cavities in the adventitious roots. At the level of meristem and root elongation zone, cortical microtubules involved in formation of trophic-type lysigenous aerenchyma were examined. For the first time, organization of tubulin microtubules in cells lining the cavities of aerenchyma was investigated. In addition, we determined the stages of programmed cell death in which microtubules are destroyed, and also compared those with published data on programmed cell death due to deprivation of sulfur, phosphorus, potassium, nitrogen, and oxygen in the nutrient medium. Cortical and endoplasmic microtubules, which constitute the main components of the plant cytoskeleton, were studied. Comparison of stepwise destruction of cortical and endoplasmic microtubules with the stages of programmed cell death revealed that endoplasmic microtubules undergo disorganization later in time than cortical ones. It is suggested that disorganization of cortical microtubules occurs at the first stages of the programmed cell death process and results in destruction of rigid cell wall, which, in turn, contributes to disruption of cytoplasmic membrane. The latter causes invaginations of the cytoplasmic membrane, which is considered to be a hallmark of early stages of cell death. It is noted that intact organization of endoplasmic microtubules persists until the final stages of cell destruction and elimination.

Keywords: aerenchyma, microtubules, programmed cell death, sulfur deficiency

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  1. Baluška F., Hasenstein K. 1997. Root cytoskeleton: Its role in perception of and response to gravity. Planta, 203(Suppl): 69–78.
  2. Bouranis D.L., Chorianopoulou S.N., SiyiannisV.F., Protonotarios V.E., Hawkesford M.J. 2003. Aerenchyma formation in roots of maize during sulphate starvation. Planta, 217: 382–391.
  3. Bouranis D., Chorianopoulou S.N., Kollias Ch., Maniou Ph., Protonotarios V., Siyiannis V., Hawkesford M.J. 2006. Dynamics of aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize. Annals of Botany, 97: 695–704.
  4. Bouranis D.L., Chorianopoulou S.N., Siyiannis V.F., Protonotarios V.E., Hawkesford M.J. 2007. Lysigenous aerenchyma development in roots – triggers and cross-talks for a cell elimination program. International Journal of Plant Developmental Biology, 1(1): 127–140.
  5. Drew M.C., He C.J., Morgan P.W. 2000. Programmed cell death and aerenchyma formation in roots. Trends in Plant Science, 5(3): 123–7.
  6. Fan M., Zhu J., Richards C., Brown K.M., Lynch J.P. 2003. Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology, 30(5): 493–506.
  7. Fagerstedt K.V. 2010. Programmed cell death and aerenchyma formation under hypoxia. In: Waterlogging signalling and tolerance in plants. Eds S. Mancuso, S. Shabala. Berlin; Heidelberg: Springer-Verlag, pp. 45–96.
  8. Gunawardena A.H., Pearce D.M., Jackson M.B., Hawes C.R., Evans D.E. 2001a. Characterisation of programmed cell death during aerenhyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212: 205–214.
  9. Gunawardena A.H., Pearce D.M., Jackson M.B., Hawes C.R., Evans D.E. 2001b. Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene. Plant Cell Environ, 24: 1369–1375.
  10. Hara-Nishimura I., Hatsugai N., Nakaune S., Kuroyanagi M., Nishimura M. 2005. Vacuolar processing enzyme, an executor of plant cell death. Current Opinion in Plant Biology, 8(4): 404–408.
  11. Hawkesford M.J. 2005. Sulphur. In: Nutritional genomics. Eds M.R. Broadley, P. White. Oxford: Blackwell Publishers, pp. 87–111.
  12. Hu B., Henry A., Brown K.M., Lynch J.P. 2014. Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays). Annals of Botany, 113(1): 181–189.
  13. Jones A. 2000. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends in Plant Science, 5(5): 225–230.
  14. Kordyum E.L., Shevchenko G.V., Brykov V.O. 2019. Cytoskeleton during aerenchyma formation in plants. Cell Biology International, 43(9): 991–998.
  15. Mollier A., Pellerin S. 1999. Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany, 50(333): 487–497.
  16. Neill S.J., Desikan R., Clarke A., Hancock J.T. 2002. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiology, 128: 13–16.
  17. Postma J.A., Lynch J.P. 2011. Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiology, 156: 1190–1201.
  18. Shevchenko G.V., Kordyum E.L. 2012. Ukrainian Botanical Journal, 69(4): 568–579.
  19. Siyiannis V.F., Protonotarios V.E., Zechmann B., Chorianopoulou S.N., Müller M., Hawkesford M.J. 2012. Comparative spatiotemporal analysis of root aerenchyma formation processes in maize due to sulphate, nitrate or phosphate deprivation. Protoplasma, 249: 671–686.
  20. Soreng R.J., Peterson P.M., Romaschenko K., Davidse G., Teisher J.K., Clark L.G., Barberá P., Gillespie L.J., Zuloaga F.O. 2017. A worldwide phylogenetic classification of the Poaceae (Gramineae) II: An update and a comparison of two 2015 classifications. Journal of Systematics and Evolution, 55(4): 259–290.
  21. van Doorn W.G. 2011. Classes of programmed cell death in plants, compared to those in animals. Journal of Experimental Botany, 62(14): 4749–4761.
  22. Visser E.J.W., Voesenek L.A.C.J. 2004. Acclimation to soil flooding– sensing and signal-transduction. Plant Soil, 254: 197–214.
  23. York L.M., Nord E.A., Lynch J.P. 2013. Integration of root phenes for soil resource acquisition. Frontiers in Plant Science, 4: 355–360.