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Aerenchyma formation in roots of maize during sulphate starvation

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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.

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Abbreviations

AOS:

active oxygen species

DDC:

N,N-diethyldithiocarbamate

PCD:

programmed cell death

SOD:

superoxide dismutase

References

  • Armstrong J, Armstrong W (1994) Chlorophyll development in mature lysigenous and schizogenous root aerenchyma provides evidence of continuing cortical cell viability. New Phytol 126:493–497

    Google Scholar 

  • Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603

    Article  CAS  PubMed  Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    CAS  PubMed  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene promoted adventitious rooting and development of cortical air spaces in Zea mays L. Planta 147:83-88

    CAS  Google Scholar 

  • 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 91:266–271

    CAS  Google Scholar 

  • Drew M, He C, Morgan P (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    CAS  PubMed  Google Scholar 

  • 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 87:9645–9649

    CAS  PubMed  Google Scholar 

  • Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414

    CAS  Google Scholar 

  • Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 199:375–384

    Article  Google Scholar 

  • 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 212:205–214

    Article  CAS  PubMed  Google Scholar 

  • 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 112:463–472

    CAS  PubMed  Google Scholar 

  • 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 98:137–142

    CAS  Google Scholar 

  • 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 165:486–492

    CAS  Google Scholar 

  • Jones AM, Dangl JL (1996) Logjam at the Styx: programmed cell death in plants. Trends Plant Sci 4:114–119

    Article  Google Scholar 

  • 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 204:277–287

    CAS  Google Scholar 

  • Kiernan JA (1999) Histological & histochemical methods. Theory & practice, 3rd edn. Butterworth Heinemann, London

  • 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 97:8849–8855

    CAS  PubMed  Google Scholar 

  • Konings H, Verschuren G (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiol Plant 49:265–270

    CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    CAS  PubMed  Google Scholar 

  • Maxwell D, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Lam E (1995) In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol 108:489–493

    CAS  Google Scholar 

  • Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497

    Article  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • 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 12:1849–1862

    CAS  PubMed  Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    CAS  Google Scholar 

  • Ros Barcheló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216

    Article  Google Scholar 

  • Rusin SE (1999) Plant microtechinque and microscopy. Oxford University Press, Oxford

  • 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 92:4158–4163

    CAS  PubMed  Google Scholar 

  • Van Breusegem F, Vranová E, Dat J, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414

    Article  Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  Google Scholar 

Download references

Acknowledgement

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

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Correspondence to D. L. Bouranis.

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Bouranis, D.L., Chorianopoulou, S.N., Siyiannis, V.F. et al. Aerenchyma formation in roots of maize during sulphate starvation. Planta 217, 382–391 (2003). https://doi.org/10.1007/s00425-003-1007-6

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  • DOI: https://doi.org/10.1007/s00425-003-1007-6

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