Planta

, Volume 217, Issue 3, pp 382–391 | Cite as

Aerenchyma formation in roots of maize during sulphate starvation

  • D. L. Bouranis
  • S. N. Chorianopoulou
  • V. F. Siyiannis
  • V. E. Protonotarios
  • M. J. Hawkesford
Original Article

Abstract

Young maize (Zea mays L., Poaceae) plants were grown in a complete, well-oxygenated nutrient solution and then deprived of their external source of sulphate. This treatment induced the formation of aerenchyma in roots. In addition to the effect of sulphate starvation on root anatomy, the presence and location of superoxide anions and hydrogen peroxide, and changes in calcium and pH were examined. By day 6 of sulphate deprivation, aerenchyma started to form in the roots of plants and the first aerenchymatous spaces were apparent in the middle of the cortex. S-starvation also induced thickening of the cell walls of the endodermis. Active oxygen species appeared in groups of intact mid-cortex cells. Formation of superoxide anion and hydrogen peroxide was found in degenerating cells of the mid-cortex. Very few nuclei in the cortex of S-starved roots fluoresced, being shrunken and near to the cell wall. By day 12 of S-deprivation, a fully developed aerenchyma was apparent and there were only a few 'chains' of cells bridging hypodermis to endodermis and stele of roots. Cell walls of endodermis of S-starved roots increased 68% in thickness. Intensive fluorescence in the cell walls of the endodermal, hypodermal and to a lesser extent of epidermal cells was observed due to the formation of active oxygen species, while there was no fluorescence in the cortical cells. There was a higher Ca concentration in the cells walls of the endodermis and epidermis, compared to the rest of the S-starved root tissues. A higher pH was observed, mainly in the cell walls of the hypodermis and to a lesser extent in the cell walls of the endodermis. Superoxide anion and hydrogen peroxide was found in degenerating cells of the root cortex. There was no fluorescence of nuclei in the cortex of S-starved roots.

Keywords

Active oxygen species Aerenchyma formation Programmed cell death Root aerenchyma Sulphate starvation Zea 

Abbreviations

AOS

active oxygen species

DDC

N,N-diethyldithiocarbamate

PCD

programmed cell death

SOD

superoxide dismutase

Notes

Acknowledgement

Rothamsted Research receives grant-aided support from the Biotechnology and Biological Science Research Council of the UK.

References

  1. Armstrong J, Armstrong W (1994) Chlorophyll development in mature lysigenous and schizogenous root aerenchyma provides evidence of continuing cortical cell viability. New Phytol 126:493–497Google Scholar
  2. Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603CrossRefPubMedGoogle Scholar
  3. Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323PubMedGoogle Scholar
  4. Drew MC, Jackson MB, Giffard S (1979) Ethylene promoted adventitious rooting and development of cortical air spaces in Zea mays L. Planta 147:83-88Google Scholar
  5. Drew MC, He CJ, Morgan PW (1989) Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate- starvation in adventitious roots of Zea mays. Plant Physiol 91:266–271Google Scholar
  6. Drew M, He C, Morgan P (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127PubMedGoogle Scholar
  7. Gehring C, Irving H, Parish R (1990) Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proc Natl Acad Sci USA 87:9645–9649PubMedGoogle Scholar
  8. Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414Google Scholar
  9. Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 199:375–384CrossRefGoogle Scholar
  10. Gunawardena A, Pearce D, Jackson M, Hawes C, Evans D (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214CrossRefPubMedGoogle Scholar
  11. He C, Morgan PW, Drew MC (1996) 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 112:463–472PubMedGoogle Scholar
  12. He CJ, Morgan PW, Drew MC (1992) Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiol 98:137–142Google Scholar
  13. Jackson MB, Fenning TM, Drew MC, Saker LR (1985) Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta 165:486–492Google Scholar
  14. Jones AM, Dangl JL (1996) Logjam at the Styx: programmed cell death in plants. Trends Plant Sci 4:114–119CrossRefGoogle Scholar
  15. Kawai M, Samarajeeva PK, Barrero RA, Nishiguchi M, Uchimiya H (1998) Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204:277–287Google Scholar
  16. Kiernan JA (1999) Histological & histochemical methods. Theory & practice, 3rd edn. Butterworth Heinemann, LondonGoogle Scholar
  17. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855PubMedGoogle Scholar
  18. Konings H, Verschuren G (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiol Plant 49:265–270Google Scholar
  19. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedGoogle Scholar
  20. Maxwell D, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276CrossRefPubMedGoogle Scholar
  21. Mittler R, Lam E (1995) In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol 108:489–493Google Scholar
  22. Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497CrossRefGoogle Scholar
  23. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395CrossRefPubMedGoogle Scholar
  24. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjärvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862PubMedGoogle Scholar
  25. Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168Google Scholar
  26. Ros Barcheló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216CrossRefGoogle Scholar
  27. Rusin SE (1999) Plant microtechinque and microscopy. Oxford University Press, OxfordGoogle Scholar
  28. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci USA 92:4158–4163PubMedGoogle Scholar
  29. Van Breusegem F, Vranová E, Dat J, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  30. Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • D. L. Bouranis
    • 1
  • S. N. Chorianopoulou
    • 1
  • V. F. Siyiannis
    • 1
  • V. E. Protonotarios
    • 1
  • M. J. Hawkesford
    • 2
  1. 1.Plant Physiology Laboratory, Department of Agricultural BiotechnologyAgricultural University of AthensAthensGreece
  2. 2.Agriculture and Environment DivisionRothamsted ResearchHarpendenUK

Personalised recommendations