Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1992 Jan;4(1):59–69. doi: 10.1105/tpc.4.1.59

Sugar Levels Modulate Differential Expression of Maize Sucrose Synthase Genes.

KE Koch 1, KD Nolte 1, ER Duke 1, DR McCarty 1, WT Avigne 1
PMCID: PMC160106  PMID: 12297629

Abstract

The two genes encoding sucrose synthase in maize (Sh1 and Sus1) show markedly different responses to changes in tissue carbohydrate status. This enzyme is widely regarded as pivotal to sucrose partitioning, import, and/or metabolism by developing plant organs. Excised maize root tips were incubated for varying periods in different sugars and a range of concentrations. The Sh1 mRNA was maximally expressed under conditions of limited carbohydrate supply (~0.2% glucose). In contrast, Sus1 transcript levels were low or nondetectable under sugar-depleted conditions and peaked at 10-fold greater glucose concentrations (2.0%). Responses to other metabolizable sugars were similar, but L-glucose and elevation of osmolarity with mannitol had little effect. Plentiful sugar supplies thus increased expression of Sus1, whereas reduced sugar availability enhanced Sh1. At the protein level, shifts in abundance of subunits encoded by Sh1 and Sus1 were much less pronounced but corresponded to changes in respective mRNA levels. Although total enzyme activity did not show net change, cellular localization of sucrose synthase protein was markedly altered. In intact roots, sucrose synthase was most prevalent in the stele and apex. In contrast, sugar depletion favored accumulation in peripheral cells, whereas high sugar levels resulted in elevated expression in all cell types. The differential response of the two sucrose synthase genes to sugars provides a potential mechanism for altering the pattern of enzyme distribution in response to changing carbohydrate status and also for adjusting the sucrose-metabolizing capacity of importing cells relative to levels of available photosynthetic products.

Full Text

The Full Text of this article is available as a PDF (4.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baysdorfer C., Vanderwoude W. J. Carbohydrate Responsive Proteins in the Roots of Pennisetum americanum. Plant Physiol. 1988 Jul;87(3):566–570. doi: 10.1104/pp.87.3.566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brouquisse R., James F., Raymond P., Pradet A. Study of glucose starvation in excised maize root tips. Plant Physiol. 1991 Jun;96(2):619–626. doi: 10.1104/pp.96.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carlson M. Regulation of sugar utilization in Saccharomyces species. J Bacteriol. 1987 Nov;169(11):4873–4877. doi: 10.1128/jb.169.11.4873-4877.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chourey P. S., Nelson O. E. The enzymatic deficiency conditioned by the shrunken-1 mutations in maize. Biochem Genet. 1976 Dec;14(11-12):1041–1055. doi: 10.1007/BF00485135. [DOI] [PubMed] [Google Scholar]
  5. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Delmer D. P. The Regulatory Properties of Purified Phaseolus aureus Sucrose Synthetase. Plant Physiol. 1972 Oct;50(4):469–472. doi: 10.1104/pp.50.4.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dennis E. S., Gerlach W. L., Pryor A. J., Bennetzen J. L., Inglis A., Llewellyn D., Sachs M. M., Ferl R. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 1984 May 11;12(9):3983–4000. doi: 10.1093/nar/12.9.3983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Echt C. S., Chourey P. S. A Comparison of Two Sucrose Synthetase Isozymes from Normal and shrunken-1 Maize. Plant Physiol. 1985 Oct;79(2):530–536. doi: 10.1104/pp.79.2.530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giaquinta R. T., Lin W., Sadler N. L., Franceschi V. R. Pathway of Phloem unloading of sucrose in corn roots. Plant Physiol. 1983 Jun;72(2):362–367. doi: 10.1104/pp.72.2.362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hattori T., Nakagawa S., Nakamura K. High-level expression of tuberous root storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium. Plant Mol Biol. 1990 Apr;14(4):595–604. doi: 10.1007/BF00027505. [DOI] [PubMed] [Google Scholar]
  11. Huber S. C., Akazawa T. A novel sucrose synthase pathway for sucrose degradation in cultured sycamore cells. Plant Physiol. 1986 Aug;81(4):1008–1013. doi: 10.1104/pp.81.4.1008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kaufman P. B., Ghosheh N. S., Lacroix J. D., Soni S. L., Ikuma H. Regulation of invertase levels in Avena stem segments by gibberellic Acid, sucrose, glucose, and fructose. Plant Physiol. 1973 Sep;52(3):221–228. doi: 10.1104/pp.52.3.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Koch K. E., Avigne W. T. Postphloem, nonvascular transfer in citrus: kinetics, metabolism, and sugar gradients. Plant Physiol. 1990 Aug;93(4):1405–1416. doi: 10.1104/pp.93.4.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Lin A. Y., Lee A. S. Induction of two genes by glucose starvation in hamster fibroblasts. Proc Natl Acad Sci U S A. 1984 Feb;81(4):988–992. doi: 10.1073/pnas.81.4.988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lowell C. A., Tomlinson P. T., Koch K. E. Sucrose-metabolizing enzymes in transport tissues and adjacent sink structures in developing citrus fruit. Plant Physiol. 1989 Aug;90(4):1394–1402. doi: 10.1104/pp.90.4.1394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Masuda H., Takahashi T., Sugawara S. Acid and alkaline invertases in suspension cultures of sugar beet cells. Plant Physiol. 1988 Jan;86(1):312–317. doi: 10.1104/pp.86.1.312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McCarty D. R., Shaw J. R., Hannah L. C. The cloning, genetic mapping, and expression of the constitutive sucrose synthase locus of maize. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9099–9103. doi: 10.1073/pnas.83.23.9099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McElfresh K. C., Chourey P. S. Anaerobiosis induces transcription but not translation of sucrose synthase in maize. Plant Physiol. 1988 Jun;87(2):542–546. doi: 10.1104/pp.87.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Nguyen-Quoc B., Krivitzky M., Huber S. C., Lecharny A. Sucrose Synthase in Developing Maize Leaves: Regulation of Activity by Protein Level during the Import to Export Transition. Plant Physiol. 1990 Oct;94(2):516–523. doi: 10.1104/pp.94.2.516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ricard B., Rivoal J., Spiteri A., Pradet A. Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol. 1991 Mar;95(3):669–674. doi: 10.1104/pp.95.3.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robbins W. J. SUCROSE AND GROWTH OF EXCISED ROOTS OF AN INBRED ZEA MAYS. Proc Natl Acad Sci U S A. 1958 Dec 15;44(12):1210–1212. doi: 10.1073/pnas.44.12.1210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saglio P. H., Pradet A. Soluble Sugars, Respiration, and Energy Charge during Aging of Excised Maize Root Tips. Plant Physiol. 1980 Sep;66(3):516–519. doi: 10.1104/pp.66.3.516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Springer B., Werr W., Starlinger P., Bennett D. C., Zokolica M., Freeling M. The Shrunken gene on chromosome 9 of Zea mays L is expressed in various plant tissues and encodes an anaerobic protein. Mol Gen Genet. 1986 Dec;205(3):461–468. doi: 10.1007/BF00338083. [DOI] [PubMed] [Google Scholar]
  29. Su J. C., Preiss J. Purification and properties of sucrose synthase from maize kernels. Plant Physiol. 1978 Mar;61(3):389–393. doi: 10.1104/pp.61.3.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sung S. J., Xu D. P., Black C. C. Identification of actively filling sucrose sinks. Plant Physiol. 1989 Apr;89(4):1117–1121. doi: 10.1104/pp.89.4.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Taliercio E. W., Chourey P. S. Post-transcriptional control of sucrose synthase expression in anaerobic seedlings of maize. Plant Physiol. 1989 Aug;90(4):1359–1364. doi: 10.1104/pp.90.4.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vyas N. K., Vyas M. N., Quiocho F. A. Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science. 1988 Dec 2;242(4883):1290–1295. doi: 10.1126/science.3057628. [DOI] [PubMed] [Google Scholar]
  33. Yang N. S., Russell D. Maize sucrose synthase-1 promoter directs phloem cell-specific expression of Gus gene in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4144–4148. doi: 10.1073/pnas.87.11.4144. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES