Aerenchyma formation in maize roots

Abstract

Maize (Zea mays L.) is generally considered to be a plant with aerenchyma formation inducible by environmental conditions. In our study, young maize plants, cultivated in various ways in order to minimise the stressing effect of hypoxia, flooding, mechanical impedance or nutrient starvation, were examined for the presence of aerenchyma in their primary roots. The area of aerenchyma in the root cortex was correlated with the root length. Although 12 different maize accessions were used, no plants without aerenchyma were acquired until an ethylene synthesis inhibitor was employed. Using an ACC-synthase inhibitor, it was confirmed that the aerenchyma formation is ethylene-regulated and dependent on irradiance. The presence of TUNEL-positive nuclei and ultrastructural changes in cortical cells suggest a connection between ethylene-dependent aerenchyma formation and programmed cell death. Position of cells with TUNEL-positive nuclei in relation to aerenchyma-channels was described.

This is a preview of subscription content, access via your institution.

Abbreviations

ACC:

1-aminocyclopropane-1-carboxylic acid

AOA:

aminooxy-acetic acid hydrochloride

PCD:

programmed cell death

References

  1. Aguilar, E.A., Turner, D.W., Sivasithamparam, K.: Aerenchyma formation in roots of four banana (Musa spp.) cultivars.-Sci. Hort. 80: 57–72, 1999.

    Article  Google Scholar 

  2. Becker, R., Ritter, A., Eichhorn, U., Lips, J., Bertram, B., Wiessler, M., Zdzienicka, M.Z., Kaina, B.: Induction of DNA breaks and apoptosis in crosslink-hypersensitive V79 cells by the cytostatic drug beta-D-glucosyl-ifosfamide mustard.-Brit. J. Cancer. 86: 130–135, 2002.

    PubMed  Article  CAS  Google Scholar 

  3. Beers, E.P., McDowell, J.M.: Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues.-Curr. Opin. Plant Biol. 4: 561–567, 2001.

    PubMed  Article  CAS  Google Scholar 

  4. Beers, E.P.: Programmed cell death during plant growth and development.-Cell Death Differ. 4: 649–661, 1997.

    PubMed  Article  CAS  Google Scholar 

  5. Bouranis, D.L., Chorianopoulou, S.N., Siyiannis, V.F., Protonotarios, V.E., Hawkesford, M.J.: Aerenchyma formation in roots of maize during sulphate starvation.-Planta 217: 382–391, 2003.

    PubMed  Article  CAS  Google Scholar 

  6. Bouranis, D.L., Chorianopoulou, S.N., Kollias, C., Maniou, P., Protonotarios, V.E., Siyiannis, V.F., Hawkesford, M.J.: Dynamics of aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize.-Ann. Bot. 97: 695–704, 2006.

    PubMed  Article  Google Scholar 

  7. Brailsford, R.W., Voesenek, L.A.C.J., Blom, C., Smith, A.R., Hall, M.A., Jackson, M.B.: Enhanced ethylene production by primary roots of Zea mays L. in response to sub-ambient partial pressures of oxygen.-Plant Cell Environ. 16: 1071–1080, 1993.

    Article  CAS  Google Scholar 

  8. Buckner, B., Janick-Buckner, D., Gray, J., Johal, G. S.: Cell-death mechanisms in maize.-Trends Plant Sci. 3: 218–223, 1998.

    Article  Google Scholar 

  9. Campbell, R., Drew, M.C.: Electron-microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage.-Planta 157: 350–357, 1983.

    Article  Google Scholar 

  10. Cohen, J.J.: Apoptosis.-Immun. Today 14: 126–130, 1993.

    PubMed  Article  CAS  Google Scholar 

  11. Colmer, T.D., Cox, M.C.H., Voesenek, L.A.C.J.: Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations.-New Phytol. 170: 767–777, 2006.

    PubMed  Article  CAS  Google Scholar 

  12. Danon, A., Delorme, V., Mailhac, N., Gallois, P.: Plant programmed cell death: a common way to die.-Plant Physiol. Biochem. 38: 647–655, 2000.

    Article  CAS  Google Scholar 

  13. De Jong, A.J., Hoeberichts, F.A., Yakimova, E.T., Maximova, E., Woltering, E.J.: Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases.-Planta 211: 656–662, 2000.

    PubMed  Article  Google Scholar 

  14. Dong, Z., Saikumar, P., Weinberg, J.M., Venkatachalam, M.A.: Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death — involvement of serine but not cysteine proteases.-Amer. J. Pathol. 151: 1205–1213, 1997.

    CAS  Google Scholar 

  15. Drew, M.C., He, C.J., Morgan, P.W.: Decreased ethylene biosynthesis and induction of aerenchyma by nitrogen-starvation or phosphate-starvation in adventitious roots of Zea mays L.-Plant Physiol. 91: 266–271, 1989.

    PubMed  Article  CAS  Google Scholar 

  16. Drew, M.C., He, C.J., Morgan, P.W.: Programmed cell death and aerenchyma formation in roots.-Trends Plant Sci. 5: 1360–1385, 2000.

    Article  Google Scholar 

  17. Ecker, J.R.: The ethylene signal-transduction pathway in plants.-Science 268: 667–675, 1995.

    PubMed  Article  CAS  Google Scholar 

  18. Enstone, D.E., Peterson, C.A.: Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions.-Plant Cell Environ. 28: 444–455, 2005.

    Article  Google Scholar 

  19. Evans, D.E.: Aerenchyma formation.-New Phytol. 161: 35–49, 2004.

    Article  Google Scholar 

  20. Finlayson, S.A., Lee, I.J., Morgan, P.W.: Phytochrome B and the regulation of circadian ethylene production in sorghum.-Plant Physiol. 116: 17–25, 1998.

    Article  CAS  Google Scholar 

  21. Finlayson, S.A., Gohil, H.L., Kato-Noguchi, H., Lee, I.J., Morgan, P.W.: Circadian ethylene synthesis in Sorghum bicolor: expression and control of the system at the whole plant level.-J. Plant Growth Regul. 23: 29–36, 2004.

    Article  CAS  Google Scholar 

  22. Gunawardena, A.H.L.A.N, Pearce, D.M.E., Jackson, M.B., Hawes, C.R. Evans, D.E.: Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).-Planta 212: 205–214, 2001a.

    PubMed  Article  CAS  Google Scholar 

  23. Gunawardena, A.H.L.A.N., Pearce, D.M.E., Jackson, M.B., Hawes, C.R., Evans, D.E.: 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, 2001b.

    Article  CAS  Google Scholar 

  24. Gunawardena, A.H.L.A.N., Greenwood, J.S., Dengler, N.G.: Programmed cell death remodels lace plant leaf shape during development.-Plant Cell 16: 60–73, 2004.

    PubMed  Article  CAS  Google Scholar 

  25. Gupta, S.D.: Plasma membrane ultrastructure in orchardgrass during NaCl stress.-Biol. Plant. 51: 759–763, 2007.

    Article  Google Scholar 

  26. He, C.J., Morgan, P.W., Drew, M.C.: Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia.-Plant Physiol. 112: 463–472, 1996.

    PubMed  CAS  Google Scholar 

  27. Jackson, M.B., Armstrong, W.: Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.-Plant Biol. 1: 274–287, 1999.

    Article  CAS  Google Scholar 

  28. Jackson, M.B., Fenning, T.M., Drew, M.C., Saker, L.R.: Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen.-Planta 165: 486–492, 1985.

    Article  CAS  Google Scholar 

  29. Jones, A.: Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?-Trends Plant Sci. 5: 225–230, 2000.

    PubMed  Article  CAS  Google Scholar 

  30. Jones, A.M., Coimbra, S., Fath, A., Sottomayor, M., Thomas, H.: Programmed cell death assays for plants.-Methods Cell Biol. 66: 437–451 2001.

    PubMed  Article  CAS  Google Scholar 

  31. Justin, S.H., Armstrong, W.: The anatomical characteristics of roots and plant response to soil flooding.-New Phytol. 106: 465–495, 1987.

    Google Scholar 

  32. Justin, S.H., Armstrong, W.: Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L).-New Phytol. 118: 49–62, 1991.

    Article  CAS  Google Scholar 

  33. Kawai, M., Samarajeewa, P.K., Barrero, R.A., Nishiguchi, M., Uchimiya, H.: Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots.-Planta 204: 277–287, 1998.

    Article  CAS  Google Scholar 

  34. Lenochová, Z., Votrubová, O., Kuthanová, A., Soukup, A., Bartáková, D.: Programmed cell death during hypoxia-induced aerenchyma formation in roots of maize.-In: Erdelská, O., Gašparíková, O., Hlinková, M., Janitor, A., Klenovská, S., Kolek, J., Krekule, J., Mistrík, I., Nátr, L. (ed.): Abstracts of 10th Days of Plant Physiology-Faculty of Natural Sciences, Comenius University, Bratislava 2004.

    Google Scholar 

  35. Lux, A., Hudák, J.: Plastid dimorphism in leaves of the terrestrial orchid, Ophrys sphegodes Miller.-New Phytol. 107: 47–51, 1987.

    Article  Google Scholar 

  36. Macháčková, I., Chauvaux, N., Dewitte, W., Van Onckelen, H.: Diurnal fluctuations in ethylene formation in Chenopodium rubrum.-Plant Physiol. 113: 981–985, 1997.

    PubMed  Google Scholar 

  37. Mano, Y., Omori, F., Takamizo, T., Kindiger, B., Bird, R.M., Loaisiga, C.H.: Variation for root aerenchyma formation in flooded and non-flooded maize and teosinte seedlings.-Plant Soil 281: 269–279, 2006.

    Article  CAS  Google Scholar 

  38. Maricle, B.R., Lee, R.W.: Aerenchyma development and oxygen transport in the estuarine cordgrasses Spartina alterniflora and S. anglica.-Aquat. Bot. 74: 109–120, 2002.

    Article  Google Scholar 

  39. Metraux, J.P., Kende, H.: The role of ethylene in the growth-response of submerged deep-water rice.-Plant Physiol. 72: 441–446, 1983.

    PubMed  Article  CAS  Google Scholar 

  40. Michalczuk, B., Rudnicki, R.M.: The effect of monochromatic red-light on ethylene production in leaves of Impatiens balsamina L. and other Species.-Plant Growth Reg. 13: 125–131, 1993.

    Article  CAS  Google Scholar 

  41. Peng, H.P., Chan, C.S., Shih, M.C., Yang, S.F.: Signalling events in the hypoxic induction of alcohol dehydrogenase gene in Arabidopsis.-Plant Physiol. 126: 742–749, 2001.

    PubMed  Article  CAS  Google Scholar 

  42. Rost, T.L.: Root tip organization and spatial relationship of differentiation events.-In: Iqbal, M. (ed.): Growth Patterns in Vascular Plants. Pp. 59–76. Dioscorides Press, Portland 1994.

    Google Scholar 

  43. Schussler, E.E., Longstreth, D.J.: Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae).-Amer. J. Bot. 87: 12–19, 2000.

    Article  Google Scholar 

  44. Van Gronsveld, J., Clijsters, H., Van Poucke, M.: Phytochrome-controlled ethylene biosynthesis of intact etiolated bean seedlings.-Planta 174: 19–24, 1988.

    Article  Google Scholar 

  45. Visser, E.J.W., Colmer, T.D., Blom, C.W.P.M., Voesenek, L.A.C.J.: Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono-and dicotyledonous wetland species with contrasting types of aerenchyma.-Plant Cell Environ. 23: 1237–1245, 2000.

    Article  Google Scholar 

  46. Voesenek, L.A.C.J., Blom, C.W.P.M.: Growth-responses of Rumex species in relation to submergence and ethylene.-Plant Cell Environ. 12: 433–439, 1989.

    Article  CAS  Google Scholar 

  47. Votrubová, O., Mašková, Z., Lenochová, Z.: Changes in growth and anatomy of maize roots following hypoxia.-Plant Soil. Environ, in press, 2009.

  48. Watkin, E.L.J., Thomson, C.J., Greenway, H.: Root development and aerenchyma formation in two wheat cultivars and one triticale cultivar grown in stagnant agar and aerated nutrient solution.-Ann. Bot. 81: 349–354, 1998.

    Article  Google Scholar 

  49. Woltering, E.J.: Death proteases come alive.-Trends Plant Sci. 9: 469–472, 2004.

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Z. Lenochová.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lenochová, Z., Soukup, A. & Votrubová, O. Aerenchyma formation in maize roots. Biol Plant 53, 263–270 (2009). https://doi.org/10.1007/s10535-009-0049-4

Download citation

Additional key words

  • Zea mays
  • hypoxia
  • ethylene
  • PCD
  • TUNEL reaction
  • TEM