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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Aug 6;93(16):8787–8791. doi: 10.1073/pnas.93.16.8787

Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator.

N Verbruggen 1, X J Hua 1, M May 1, M Van Montagu 1
PMCID: PMC38752  PMID: 8710950

Abstract

In many plants, osmotic stress induces a rapid accumulation of proline through de novo synthesis from glutamate. This response is thought to play a pivotal role in osmotic stress tolerance [Kishor, P. B. K., Hong, Z., Miao, G.-H., Hu, C.-A. A. and Verma, D. P. S. (1995) Plant Physiol. 108, 1387-1394]. During recovery from osmotic stress, accumulated proline is rapidly oxidized to glutamate and the first step of this process is catalyzed by proline oxidase. We have isolated a full-length cDNA from Arabidopsis thaliana, At-POX, which maps to a single locus on chromosome 3 and that encodes a predicted polypeptide of 499 amino acids showing significant similarity with proline oxidase sequences from Drosophila and Saccharomyces cerevisiae (55.5% and 45.1%, respectively). The predicted location of the encoded polypeptide is the inner mitochondrial membrane. RNA gel blot analysis revealed that At-POX mRNA levels declined rapidly upon osmotic stress and this decline preceded proline accumulation. On the other hand, At-POX mRNA levels rapidly increased during recovery. Free proline, exogenously added to plants, was found to be an effective inducer of At-POX expression; indeed, At-POX was highly expressed in flowers and mature seeds where the proline level is higher relative to other organs of Arabidopsis. Our results indicate that stress- and developmentally derived signals interact to determine proline homeostasis in Arabidopsis.

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Selected References

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  1. Brunner G., Neupert W. Localisation of proline oxidase and Delta-pyrroline-5-carboxylic acid dehydrogenase in rat liver. FEBS Lett. 1969 Jun;3(4):283–286. doi: 10.1016/0014-5793(69)80159-6. [DOI] [PubMed] [Google Scholar]
  2. Coschigano P. W., Magasanik B. The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to glutathione s-transferases. Mol Cell Biol. 1991 Feb;11(2):822–832. doi: 10.1128/mcb.11.2.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Elthon T. E., Stewart C. R. Proline Oxidation in Corn Mitochondria : Involvement of NAD, Relationship to Ornithine Metabolism, and Sidedness on the Inner Membrane. Plant Physiol. 1982 Aug;70(2):567–572. doi: 10.1104/pp.70.2.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gavel Y., von Heijne G. Cleavage-site motifs in mitochondrial targeting peptides. Protein Eng. 1990 Oct;4(1):33–37. doi: 10.1093/protein/4.1.33. [DOI] [PubMed] [Google Scholar]
  5. Gosti F., Bertauche N., Vartanian N., Giraudat J. Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet. 1995 Jan 6;246(1):10–18. doi: 10.1007/BF00290128. [DOI] [PubMed] [Google Scholar]
  6. Hayward D. C., Delaney S. J., Campbell H. D., Ghysen A., Benzer S., Kasprzak A. B., Cotsell J. N., Young I. G., Miklos G. L. The sluggish-A gene of Drosophila melanogaster is expressed in the nervous system and encodes proline oxidase, a mitochondrial enzyme involved in glutamate biosynthesis. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2979–2983. doi: 10.1073/pnas.90.7.2979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Holden J. S. Free amino acid levels in the cockroach, Periplaneta americana. J Physiol. 1973 Jul;232(2):61P–62P. [PubMed] [Google Scholar]
  8. Karchi H., Shaul O., Galili G. Lysine synthesis and catabolism are coordinately regulated during tobacco seed development. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2577–2581. doi: 10.1073/pnas.91.7.2577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kishor PBK., Hong Z., Miao G. H., Hu CAA., Verma DPS. Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol. 1995 Aug;108(4):1387–1394. doi: 10.1104/pp.108.4.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  11. Ling M., Allen S. W., Wood J. M. Sequence analysis identifies the proline dehydrogenase and delta 1-pyrroline-5-carboxylate dehydrogenase domains of the multifunctional Escherichia coli PutA protein. J Mol Biol. 1994 Nov 11;243(5):950–956. doi: 10.1006/jmbi.1994.1696. [DOI] [PubMed] [Google Scholar]
  12. Maloy S. R., Roth J. R. Regulation of proline utilization in Salmonella typhimurium: characterization of put::Mu d(Ap, lac) operon fusions. J Bacteriol. 1983 May;154(2):561–568. doi: 10.1128/jb.154.2.561-568.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mauch F., Dudler R. Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 1993 Aug;102(4):1193–1201. doi: 10.1104/pp.102.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Meyer R. C., Jr, Goldsbrough P. B., Woodson W. R. An ethylene-responsive flower senescence-related gene from carnation encodes a protein homologous to glutathione S-transferases. Plant Mol Biol. 1991 Aug;17(2):277–281. doi: 10.1007/BF00039505. [DOI] [PubMed] [Google Scholar]
  15. Savouré A., Jaoua S., Hua X. J., Ardiles W., Van Montagu M., Verbruggen N. Isolation, characterization, and chromosomal location of a gene encoding the delta 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett. 1995 Sep 18;372(1):13–19. doi: 10.1016/0014-5793(95)00935-3. [DOI] [PubMed] [Google Scholar]
  16. Stewart C. R. Proline Content and Metabolism during Rehydration of Wilted Excised Leaves in the Dark. Plant Physiol. 1972 Dec;50(6):679–681. doi: 10.1104/pp.50.6.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Verbruggen N., Villarroel R., Van Montagu M. Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol. 1993 Nov;103(3):771–781. doi: 10.1104/pp.103.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Wang S. S., Brandriss M. C. Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT1 gene. Mol Cell Biol. 1986 Jul;6(7):2638–2645. doi: 10.1128/mcb.6.7.2638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wang S. S., Brandriss M. C. Proline utilization in Saccharomyces cerevisiae: sequence, regulation, and mitochondrial localization of the PUT1 gene product. Mol Cell Biol. 1987 Dec;7(12):4431–4440. doi: 10.1128/mcb.7.12.4431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Xu S., Falvey D. A., Brandriss M. C. Roles of URE2 and GLN3 in the proline utilization pathway in Saccharomyces cerevisiae. Mol Cell Biol. 1995 Apr;15(4):2321–2330. doi: 10.1128/mcb.15.4.2321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Yoshiba Y., Kiyosue T., Katagiri T., Ueda H., Mizoguchi T., Yamaguchi-Shinozaki K., Wada K., Harada Y., Shinozaki K. Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J. 1995 May;7(5):751–760. doi: 10.1046/j.1365-313x.1995.07050751.x. [DOI] [PubMed] [Google Scholar]

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