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. 1997 Aug;114(4):1215–1224. doi: 10.1104/pp.114.4.1215

Developmental regulation of pyrroline-5-carboxylate reductase gene expression in Arabidopsis.

X J Hua 1, B van de Cotte 1, M Van Montagu 1, N Verbruggen 1
PMCID: PMC158414  PMID: 9276946

Abstract

At-P5R, a gene encoding the last enzyme of the proline (Pro) biosynthetic pathway in Arabidopsis thaliana, is developmentally regulated. To characterize the cis elements responsible for this developmental regulation, a series of 5' deletions of the At-P5R promoter were transcriptionally fused to a beta-glucuronidase (GUS)-coding region and transformed into Arabidopsis. The complete promoter of At-P5R directs strong GUS activity in root tips, the shoot meristem, guard cells, hydathodes, pollen grains, ovules, and developing seeds, all of which contain rapidly dividing cells and/or are undergoing changes in osmotic potential. This expression pattern is consistent with the function of Pro as an energy, nitrogen, and carbon source and as an osmoticum in response to dehydration. Promoters longer than 212 base pairs (bp) showed the same expression pattern, whereas those shorter than 143 bp did not direct any detectable GUS activity in any organs. This suggests that a 69-bp promoter region located between -212 and -143 bp is necessary to establish the tissue-specific expression of At-P5R during development. The Pro content measured in different organs suggests that, in addition to transcriptional control of the biosynthetic pathway, the transport of Pro may play a role in its distribution within Arabidopsis. Several aspects of the relationship between Pro metabolism and plant physiology are discussed.

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Selected References

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  1. Adams E., Frank L. Metabolism of proline and the hydroxyprolines. Annu Rev Biochem. 1980;49:1005–1061. doi: 10.1146/annurev.bi.49.070180.005041. [DOI] [PubMed] [Google Scholar]
  2. Benfey P. N., Chua N. H. The Cauliflower Mosaic Virus 35S Promoter: Combinatorial Regulation of Transcription in Plants. Science. 1990 Nov 16;250(4983):959–966. doi: 10.1126/science.250.4983.959. [DOI] [PubMed] [Google Scholar]
  3. Buhl M. B., Stewart C. R. Effects of NaCl on Proline Synthesis and Utilization in Excised Barley Leaves. Plant Physiol. 1983 Jul;72(3):664–667. doi: 10.1104/pp.72.3.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Delauney A. J., Hu C. A., Kishor P. B., Verma D. P. Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem. 1993 Sep 5;268(25):18673–18678. [PubMed] [Google Scholar]
  5. Delauney A. J., Verma D. P. A soybean gene encoding delta 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet. 1990 May;221(3):299–305. doi: 10.1007/BF00259392. [DOI] [PubMed] [Google Scholar]
  6. Eyal Y., Curie C., McCormick S. Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell. 1995 Mar;7(3):373–384. doi: 10.1105/tpc.7.3.373. [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. Hu C. A., Delauney A. J., Verma D. P. A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9354–9358. doi: 10.1073/pnas.89.19.9354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kaldenhoff R., Kölling A., Meyers J., Karmann U., Ruppel G., Richter G. The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J. 1995 Jan;7(1):87–95. doi: 10.1046/j.1365-313x.1995.07010087.x. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Ondek B., Shepard A., Herr W. Discrete elements within the SV40 enhancer region display different cell-specific enhancer activities. EMBO J. 1987 Apr;6(4):1017–1025. doi: 10.1002/j.1460-2075.1987.tb04854.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Paleg L. G., Stewart G. R., Bradbeer J. W. Proline and glycine betaine influence protein solvation. Plant Physiol. 1984 Aug;75(4):974–978. doi: 10.1104/pp.75.4.974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Raghothama K. G., Liu D., Nelson D. E., Hasegawa P. M., Bressan R. A. Analysis of an osmotically regulated pathogenesis-related osmotin gene promoter. Plant Mol Biol. 1993 Dec;23(6):1117–1128. doi: 10.1007/BF00042346. [DOI] [PubMed] [Google Scholar]
  15. Rhodes D., Handa S., Bressan R. A. Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol. 1986 Dec;82(4):890–903. doi: 10.1104/pp.82.4.890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Samac D. A., Shah D. M. Developmental and Pathogen-Induced Activation of the Arabidopsis Acidic Chitinase Promoter. Plant Cell. 1991 Oct;3(10):1063–1072. doi: 10.1105/tpc.3.10.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Szoke A., Miao G. H., Hong Z., Verma D. P. Subcellular location of delta-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean. Plant Physiol. 1992 Aug;99(4):1642–1649. doi: 10.1104/pp.99.4.1642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Verbruggen N., Hua X. J., May M., Van Montagu M. Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8787–8791. doi: 10.1073/pnas.93.16.8787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Walton E. F., Clark C. J., Boldingh H. L. Effect of Hydrogen Cyanamide on Amino Acid Profiles in Kiwifruit Buds during Budbreak. Plant Physiol. 1991 Nov;97(3):1256–1259. doi: 10.1104/pp.97.3.1256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wang H., Cutler A. J. Promoters from kin1 and cor6.6, two Arabidopsis thaliana low-temperature- and ABA-inducible genes, direct strong beta-glucuronidase expression in guard cells, pollen and young developing seeds. Plant Mol Biol. 1995 Jul;28(4):619–634. doi: 10.1007/BF00021188. [DOI] [PubMed] [Google Scholar]
  24. Weterings K., Schrauwen J., Wullems G., Twell D. Functional dissection of the promoter of the pollen-specific gene NTP303 reveals a novel pollen-specific, and conserved cis-regulatory element. Plant J. 1995 Jul;8(1):55–63. doi: 10.1046/j.1365-313x.1995.08010055.x. [DOI] [PubMed] [Google Scholar]
  25. van Buul P. P., Goudzwaard J. H. The relation between induced reciprocal translocations and cell killing of mouse spermatogonial stem cells after combined treatments with hydroxyurea and X-rays. Mutat Res. 1990 Apr;243(4):259–266. doi: 10.1016/0165-7992(90)90141-6. [DOI] [PubMed] [Google Scholar]

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