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. 1995 Aug;108(4):1647–1656. doi: 10.1104/pp.108.4.1647

End-Product Control of Carbon Metabolism in Culture-Grown Sugar Beet Plants (Molecular and Physiological Evidence on Accelerated Leaf Development and Enhanced Gene Expression).

Y Kovtun 1, J Daie 1
PMCID: PMC157546  PMID: 12228569

Abstract

Sugar beet (Beta vulgaris L.) seedlings were grown on media containing 90 to 300 mM sucrose or glucose. Compared to controls, sugar-grown plants had higher growth rate, photosynthesis, and leaf sugar levels. The steady-state level of transcripts increased significantly for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) (rbcS) and the cytosolic fructose-1,6-bisphosphatase and moderately for the Rubisco large subunit (rbcL). The transcript level of sucrose phosphate synthase remained unchanged. Fructose-1,6-bisphosphatase and Rubisco activities did not change in the presence of sugars, but that of sucrose phosphate synthase increased (44 and 90% under selective and nonselective assay conditions, respectively). Accelerated leaf development was indicated by (a) autoradiograms of leaves that showed that sucrose loading occurred earlier, (b) export capacity that also occurred earlier but, after about 2 weeks, differences were not detectable, and (c) sucrose synthase activity that declined significantly. Several conclusions emerged: (a) response was nonosmotic and gene and sugar specific, (b) sugars caused accelerated leaf development and sink-to-source transition, (c) enhanced gene expression was due to advanced leaf development, and (d) whereas Rubisco and cytosolic fructose-1,6-bisphosphatase genes were sugar repressed in mature leaves of greenhouse-grown plants, they were unaffected in mature, culture-grown leaves. To our knowledge, these data provide the first evidence in higher plants that, depending on the physiological/developmental context of leaves, sugars lead to differential regulation of the same gene.

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Selected References

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  1. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. Brusslan J. A., Tobin E. M. Light-independent developmental regulation of cab gene expression in Arabidopsis thaliana seedlings. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7791–7795. doi: 10.1073/pnas.89.16.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheng C. L., Acedo G. N., Cristinsin M., Conkling M. A. Sucrose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1861–1864. doi: 10.1073/pnas.89.5.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Diamond M. I., Miner J. N., Yoshinaga S. K., Yamamoto K. R. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990 Sep 14;249(4974):1266–1272. doi: 10.1126/science.2119054. [DOI] [PubMed] [Google Scholar]
  8. Dickinson C. D., Altabella T., Chrispeels M. J. Slow-growth phenotype of transgenic tomato expressing apoplastic invertase. Plant Physiol. 1991 Feb;95(2):420–425. doi: 10.1104/pp.95.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Galtier N., Foyer C. H., Huber J., Voelker T. A., Huber S. C. Effects of Elevated Sucrose-Phosphate Synthase Activity on Photosynthesis, Assimilate Partitioning, and Growth in Tomato (Lycopersicon esculentum var UC82B). Plant Physiol. 1993 Feb;101(2):535–543. doi: 10.1104/pp.101.2.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goldschmidt E. E., Huber S. C. Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol. 1992 Aug;99(4):1443–1448. doi: 10.1104/pp.99.4.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Huang N., Chandler J., Thomas B. R., Koizumi N., Rodriguez R. L. Metabolic regulation of alpha-amylase gene expression in transgenic cell cultures of rice (Oryza sativa L.). Plant Mol Biol. 1993 Nov;23(4):737–747. doi: 10.1007/BF00021529. [DOI] [PubMed] [Google Scholar]
  12. Huber S. C., Huber J. L. Role of sucrose-phosphate synthase in sucrose metabolism in leaves. Plant Physiol. 1992 Aug;99(4):1275–1278. doi: 10.1104/pp.99.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lenz A. G., Holzer H. Rapid reversible inactivation of fructose-1,6-bisphosphatase in Saccharomyces cerivisiae by glucose. FEBS Lett. 1980 Jan 14;109(2):271–274. doi: 10.1016/0014-5793(80)81103-3. [DOI] [PubMed] [Google Scholar]
  14. Maas C., Schaal S., Werr W. A feedback control element near the transcription start site of the maize Shrunken gene determines promoter activity. EMBO J. 1990 Nov;9(11):3447–3452. doi: 10.1002/j.1460-2075.1990.tb07552.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McKendree W. L., Jr, Ferl R. J. Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol Biol. 1992 Aug;19(5):859–862. doi: 10.1007/BF00027081. [DOI] [PubMed] [Google Scholar]
  16. Miesfeld R., Godowski P. J., Maler B. A., Yamamoto K. R. Glucocorticoid receptor mutants that define a small region sufficient for enhancer activation. Science. 1987 Apr 24;236(4800):423–427. doi: 10.1126/science.3563519. [DOI] [PubMed] [Google Scholar]
  17. Morell M., Copeland L. Sucrose synthase of soybean nodules. Plant Physiol. 1985 May;78(1):149–154. doi: 10.1104/pp.78.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Müller-Röber B. T., Kossmann J., Hannah L. C., Willmitzer L., Sonnewald U. One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet. 1990 Oct;224(1):136–146. doi: 10.1007/BF00259460. [DOI] [PubMed] [Google Scholar]
  19. Sakai D. D., Helms S., Carlstedt-Duke J., Gustafsson J. A., Rottman F. M., Yamamoto K. R. Hormone-mediated repression: a negative glucocorticoid response element from the bovine prolactin gene. Genes Dev. 1988 Sep;2(9):1144–1154. doi: 10.1101/gad.2.9.1144. [DOI] [PubMed] [Google Scholar]
  20. Salanoubat M., Belliard G. The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose concentration. Gene. 1989 Dec 7;84(1):181–185. doi: 10.1016/0378-1119(89)90153-4. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Takeda S., Mano S., Ohto Ma., Nakamura K. Inhibitors of Protein Phosphatases 1 and 2A Block the Sugar-Inducible Gene Expression in Plants. Plant Physiol. 1994 Oct;106(2):567–574. doi: 10.1104/pp.106.2.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wang J. L., Turgeon R., Carr J. P., Berry J. O. Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant. Plant Cell. 1993 Mar;5(3):289–296. doi: 10.1105/tpc.5.3.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Worrell A. C., Bruneau J. M., Summerfelt K., Boersig M., Voelker T. A. Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. Plant Cell. 1991 Oct;3(10):1121–1130. doi: 10.1105/tpc.3.10.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. el-Maghrabi M. R., Pilkis J., Marker A. J., Colosia A. D., D'Angelo G., Fraser B. A., Pilkis S. J. cDNA sequence of rat liver fructose-1,6-bisphosphatase and evidence for down-regulation of its mRNA by insulin. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8430–8434. doi: 10.1073/pnas.85.22.8430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. van der Steege G., Nieboer M., Swaving J., Tempelaar M. J. Potato granule-bound starch synthase promoter-controlled GUS expression: regulation of expression after transient and stable transformation. Plant Mol Biol. 1992 Oct;20(1):19–30. doi: 10.1007/BF00029145. [DOI] [PubMed] [Google Scholar]

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