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. 1996 May;111(1):243–257. doi: 10.1104/pp.111.1.243

Transgenic AEQUORIN reveals organ-specific cytosolic Ca2+ responses to anoxia and Arabidopsis thaliana seedlings.

J C Sedbrook 1, P J Kronebusch 1, G G Borisy 1, A J Trewavas 1, P H Masson 1
PMCID: PMC157832  PMID: 8685265

Abstract

Using the transgenic AEQUORIN system, we showed that the cotyledons and leaves of Arabidopsis thaliana seedlings developed a biphasic luminescence response to anoxia, indicating changes in cytosolic Ca2+ levels. A fast and transient luminescence peak occurred within minutes of anoxia, followed by a second, prolonged luminescence response that lasted 1.5 to 4 h. The Ca2+ channel blockers Gd3+, La3+, and ruthenium red (RR) partially inhibited the first response and promoted a larger and earlier second response, suggesting different origins for these responses. Both Gd3+ and RR also partially inhibited anaerobic induction of alcohol dehydrogenase gene expression. However, although anaerobic alcohol dehydrogenase gene induction occurred in seedlings exposed to water-agar medium and in roots, related luminescence responses were absent. Upon return to normoxia, the luminescence of cotyledons, leaves, and roots dropped quickly, before increasing again in a Gd3+, La3+, ethyleneglycol-bis(beta-aminoethyl ether)-N,N'-tetraacetic acid-, and RR-sensitive fashion.

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Selected References

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  1. Allshire A., Piper H. M., Cuthbertson K. S., Cobbold P. H. Cytosolic free Ca2+ in single rat heart cells during anoxia and reoxygenation. Biochem J. 1987 Jun 1;244(2):381–385. doi: 10.1042/bj2440381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chang C., Meyerowitz E. M. Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1408–1412. doi: 10.1073/pnas.83.5.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. DeLisle A. J., Ferl R. J. Transcriptional control of alcohol dehydrogenase genes in plants. Int Rev Cytol. 1990;123:39–60. doi: 10.1016/s0074-7696(08)60670-1. [DOI] [PubMed] [Google Scholar]
  4. Farber J. L. The role of calcium ions in toxic cell injury. Environ Health Perspect. 1990 Mar;84:107–111. doi: 10.1289/ehp.9084107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gasbarrini A., Borle A. B., Farghali H., Francavilla A., Van Thiel D. Fructose protects rat hepatocytes from anoxic injury. Effect on intracellular ATP, Ca2+i, Mg2+i, Na+i, and pHi. J Biol Chem. 1992 Apr 15;267(11):7545–7552. [PubMed] [Google Scholar]
  6. Knight M. R., Read N. D., Campbell A. K., Trewavas A. J. Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins. J Cell Biol. 1993 Apr;121(1):83–90. doi: 10.1083/jcb.121.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Martin T., Frommer W. B., Salanoubat M., Willmitzer L. Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J. 1993 Aug;4(2):367–377. doi: 10.1046/j.1365-313x.1993.04020367.x. [DOI] [PubMed] [Google Scholar]
  8. Masson P., Rutherford G., Banks J. A., Fedoroff N. Essential large transcripts of the maize Spm transposable element are generated by alternative splicing. Cell. 1989 Aug 25;58(4):755–765. doi: 10.1016/0092-8674(89)90109-8. [DOI] [PubMed] [Google Scholar]
  9. Miyata H., Lakatta E. G., Stern M. D., Silverman H. S. Relation of mitochondrial and cytosolic free calcium to cardiac myocyte recovery after exposure to anoxia. Circ Res. 1992 Sep;71(3):605–613. doi: 10.1161/01.res.71.3.605. [DOI] [PubMed] [Google Scholar]
  10. Monk L. S., Fagerstedt K. V., Crawford R. M. Superoxide Dismutase as an Anaerobic Polypeptide : A Key Factor in Recovery from Oxygen Deprivation in Iris pseudacorus? Plant Physiol. 1987 Dec;85(4):1016–1020. doi: 10.1104/pp.85.4.1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Neuhaus G., Bowler C., Kern R., Chua N. H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993 Jun 4;73(5):937–952. doi: 10.1016/0092-8674(93)90272-r. [DOI] [PubMed] [Google Scholar]
  12. Nicotera P., Bellomo G., Orrenius S. Calcium-mediated mechanisms in chemically induced cell death. Annu Rev Pharmacol Toxicol. 1992;32:449–470. doi: 10.1146/annurev.pa.32.040192.002313. [DOI] [PubMed] [Google Scholar]
  13. Peschke V. M., Sachs M. M. Characterization and expression of transcripts induced by oxygen deprivation in maize (Zea mays L.). Plant Physiol. 1994 Feb;104(2):387–394. doi: 10.1104/pp.104.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Poovaiah B. W., Reddy A. S. Calcium and signal transduction in plants. CRC Crit Rev Plant Sci. 1993;12(3):185–211. doi: 10.1080/07352689309701901. [DOI] [PubMed] [Google Scholar]
  15. Price A. H., Taylor A., Ripley S. J., Griffiths A., Trewavas A. J., Knight M. R. Oxidative Signals in Tobacco Increase Cytosolic Calcium. Plant Cell. 1994 Sep;6(9):1301–1310. doi: 10.1105/tpc.6.9.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Roberts J. K., Hooks M. A., Miaullis A. P., Edwards S., Webster C. Contribution of Malate and Amino Acid Metabolism to Cytoplasmic pH Regulation in Hypoxic Maize Root Tips Studied Using Nuclear Magnetic Resonance Spectroscopy. Plant Physiol. 1992 Feb;98(2):480–487. doi: 10.1104/pp.98.2.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sachs M. M., Freeling M., Okimoto R. The anaerobic proteins of maize. Cell. 1980 Jul;20(3):761–767. doi: 10.1016/0092-8674(80)90322-0. [DOI] [PubMed] [Google Scholar]
  18. Saint-Ges V., Roby C., Bligny R., Pradet A., Douce R. Kinetic studies of the variations of cytoplasmic pH, nucleotide triphosphates (31P-NMR) and lactate during normoxic and anoxic transitions in maize root tips. Eur J Biochem. 1991 Sep 1;200(2):477–482. doi: 10.1111/j.1432-1033.1991.tb16207.x. [DOI] [PubMed] [Google Scholar]
  19. Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990 Oct;2(10):1027–1038. doi: 10.1105/tpc.2.10.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Subbaiah C. C., Bush D. S., Sachs M. M. Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell. 1994 Dec;6(12):1747–1762. doi: 10.1105/tpc.6.12.1747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Subbaiah C. C., Zhang J., Sachs M. M. Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiol. 1994 May;105(1):369–376. doi: 10.1104/pp.105.1.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yang Y., Kwon H. B., Peng H. P., Shih M. C. Stress responses and metabolic regulation of glyceraldehyde-3-phosphate dehydrogenase genes in Arabidopsis. Plant Physiol. 1993 Jan;101(1):209–216. doi: 10.1104/pp.101.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]

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