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. 1993 Oct;103(2):441–448. doi: 10.1104/pp.103.2.441

Long-term anoxia tolerance. Multi-level regulation of gene expression in the amphibious plant Acorus calamus L.

M Bucher 1, C Kuhlemeier 1
PMCID: PMC159002  PMID: 8029333

Abstract

Acorus calamus is a monocotyledonous wetland plant that can withstand extremely long periods of anoxia. We have investigated the expression of genes coding for pyruvate decarboxylase (Pdc), alcohol dehydrogenase (Adh), and fructose-1,6-bisphosphate aldolase (Ald) during periods of anoxia ranging from 2 h to 2 months. Upon anoxic incubation, Pdc mRNA levels peak at 6 h, followed by Adh and Ald, which peak at 12 and 72 h, respectively. Subsequently, the mRNA levels of all three genes decline within days to low levels. In contrast, alcohol dehydrogenase (ADH) protein levels increase steadily for at least a week and then remain constant. Native gel electrophoresis demonstrates the presence of two sets of ADH isozymes, one present constitutively, the other enhanced during anoxia. Translation initiation factor 4A protein levels, used as a control, remain constant during 2 months of anoxia. The results suggest that A. calamus has developed a complex anaerobic response consisting of differential regulation of transcription, translation, and posttranslational processes.

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Selected References

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  1. Andrews D. L., Cobb B. G., Johnson J. R., Drew M. C. Hypoxic and Anoxic Induction of Alcohol Dehydrogenase in Roots and Shoots of Seedlings of Zea mays (Adh Transcripts and Enzyme Activity). Plant Physiol. 1993 Feb;101(2):407–414. doi: 10.1104/pp.101.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bailey-Serres J., Freeling M. Hypoxic stress-induced changes in ribosomes of maize seedling roots. Plant Physiol. 1990 Nov;94(3):1237–1243. doi: 10.1104/pp.94.3.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boylen C. W., Sheldon R. B. Submergent macrophytes: growth under winter ice cover. Science. 1976 Nov 19;194(4267):841–842. doi: 10.1126/science.194.4267.841. [DOI] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  5. Chamot D., Kuhlemeier C. Differential expression of genes encoding the hypusine-containing translation initiation factor, eIF-5A, in tobacco. Nucleic Acids Res. 1992 Feb 25;20(4):665–669. doi: 10.1093/nar/20.4.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Constabel C. P., Matton D. P., Brisson N. Concurrent synthesis and degradation of alcohol dehydrogenase in elicitor-treated and wounded potato tubers. Plant Physiol. 1990 Nov;94(3):887–891. doi: 10.1104/pp.94.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dennis E. S., Sachs M. M., Gerlach W. L., Finnegan E. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize. Nucleic Acids Res. 1985 Feb 11;13(3):727–743. doi: 10.1093/nar/13.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hake S., Kelley P. M., Taylor W. C., Freeling M. Coordinate induction of alcohol dehydrogenase 1, aldolase, and other anaerobic RNAs in maize. J Biol Chem. 1985 Apr 25;260(8):5050–5054. [PubMed] [Google Scholar]
  9. Hanson A. D., Jacobsen J. V., Zwar J. A. Regulated expression of three alcohol dehydrogenase genes in barley aleurone layers. Plant Physiol. 1984 Jul;75(3):573–581. doi: 10.1104/pp.75.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hole D. J., Cobb B. G., Hole P. S., Drew M. C. Enhancement of Anaerobic Respiration in Root Tips of Zea mays following Low-Oxygen (Hypoxic) Acclimation. Plant Physiol. 1992 May;99(1):213–218. doi: 10.1104/pp.99.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kelley P. M., Freeling M. Anaerobic expression of maize fructose-1,6-diphosphate aldolase. J Biol Chem. 1984 Nov 25;259(22):14180–14183. [PubMed] [Google Scholar]
  12. Kelley P. M. Maize pyruvate decarboxylase mRNA is induced anaerobically. Plant Mol Biol. 1989 Aug;13(2):213–222. doi: 10.1007/BF00016139. [DOI] [PubMed] [Google Scholar]
  13. Kelley P. M., Tolan D. R. The complete amino Acid sequence for the anaerobically induced aldolase from maize derived from cDNA clones. Plant Physiol. 1986 Dec;82(4):1076–1080. doi: 10.1104/pp.82.4.1076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kuhlemeier C. Transcriptional and post-transcriptional regulation of gene expression in plants. Plant Mol Biol. 1992 May;19(1):1–14. doi: 10.1007/978-94-011-2656-4_1. [DOI] [PubMed] [Google Scholar]
  15. Opik H. Effect of anaerobiosis on respiratory rate, cytochrome oxidase activity and mitochondrial structures in coleoptiles of rice (Oryza sativa L.). J Cell Sci. 1973 May;12(3):725–739. doi: 10.1242/jcs.12.3.725. [DOI] [PubMed] [Google Scholar]
  16. Owttrim G. W., Hofmann S., Kuhlemeier C. Divergent genes for translation initiation factor eIF-4A are coordinately expressed in tobacco. Nucleic Acids Res. 1991 Oct 25;19(20):5491–5496. doi: 10.1093/nar/19.20.5491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Roberts J. K., Callis J., Jardetzky O., Walbot V., Freeling M. Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6029–6033. doi: 10.1073/pnas.81.19.6029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Russell D. A., Sachs M. M. Differential expression and sequence analysis of the maize glyceraldehyde-3-phosphate dehydrogenase gene family. Plant Cell. 1989 Aug;1(8):793–803. doi: 10.1105/tpc.1.8.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Saglio P. H., Raymond P., Pradet A. Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia: CONTROL BY SOLUBLE SUGARS. Plant Physiol. 1980 Dec;66(6):1053–1057. doi: 10.1104/pp.66.6.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shimomura S., Beevers H. Alcohol dehydrogenase and an inactivator from rice seedlings. Plant Physiol. 1983 Apr;71(4):736–741. doi: 10.1104/pp.71.4.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]

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