Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1996 Oct;112(2):473–482. doi: 10.1104/pp.112.2.473

Tissue-Specific and Light-Mediated Expression of the C4 Photosynthetic NAD-Dependent Malic Enzyme of Amaranth Mitochondria.

J J Long 1, J O Berry 1
PMCID: PMC157970  PMID: 12226404

Abstract

In the C4 dicotyledonous grain plant amaranth (Amaranthus hypochondriacus), a mitochondrial NAD-dependent malic enzyme (NAD-ME; EC 1.1.1.39) serves a specialized and essential role in photosynthetic carbon fixation. In this study we have examined specialized photosynthetic gene expression patterns for the NAD-ME [alpha] subunit. We show here that the [alpha] subunit gene is preferentially expressed in leaves and cotyledons (the most photosynthetically active tissues), and this expression is specific to the bundle-sheath cells of these tissues from the earliest stages of development. Synthesis of the [alpha] subunit polypeptide and accumulation of its corresponding mRNA are strongly light-dependent, but this regulation is also influenced by seedling development. In addition, light-dependent accumulation of the [alpha] subunit mRNA is regulated at transcriptional as well as posttranscriptional levels. Our findings demonstrate that the NAD-ME of amaranth has acquired numerous complex tissue-specific and light-mediated regulation patterns that define its specialized function as a key enzyme in the C4 photosynthetic pathway.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

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

  1. Berry J. O., Breiding D. E., Klessig D. F. Light-mediated control of translational initiation of ribulose-1, 5-bisphosphate carboxylase in amaranth cotyledons. Plant Cell. 1990 Aug;2(8):795–803. doi: 10.1105/tpc.2.8.795. [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. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol. 1986 Jul;6(7):2347–2353. doi: 10.1128/mcb.6.7.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collins P. D., Hague D. R. Light-stimulated synthesis of NADP malic enzyme in leaves of maize. J Biol Chem. 1983 Mar 25;258(6):4012–4018. [PubMed] [Google Scholar]
  5. Fluhr R., Kuhlemeier C., Nagy F., Chua N. H. Organ-specific and light-induced expression of plant genes. Science. 1986 May 30;232(4754):1106–1112. doi: 10.1126/science.232.4754.1106. [DOI] [PubMed] [Google Scholar]
  6. Furbank R. T., Taylor W. C. Regulation of Photosynthesis in C3 and C4 Plants: A Molecular Approach. Plant Cell. 1995 Jul;7(7):797–807. doi: 10.1105/tpc.7.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hatch M. D., Mau S. L., Kagawa T. Properties of leaf NAD malic enzyme from plants with C4 pathway photosynthesis. Arch Biochem Biophys. 1974 Nov;165(1):188–200. doi: 10.1016/0003-9861(74)90155-6. [DOI] [PubMed] [Google Scholar]
  8. Langdale J. A., Metzler M. C., Nelson T. The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. Dev Biol. 1987 Jul;122(1):243–255. doi: 10.1016/0012-1606(87)90349-6. [DOI] [PubMed] [Google Scholar]
  9. Long J. J., Wang J. L., Berry J. O. Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. J Biol Chem. 1994 Jan 28;269(4):2827–2833. [PubMed] [Google Scholar]
  10. Ramsperger V. C., Summers R. G., Berry J. O. Photosynthetic Gene Expression in Meristems and during Initial Leaf Development in a C4 Dicotyledonous Plant. Plant Physiol. 1996 Aug;111(4):999–1010. doi: 10.1104/pp.111.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Schäffner A. R., Sheen J. Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell. 1991 Sep;3(9):997–1012. doi: 10.1105/tpc.3.9.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Sheen J. Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell. 1991 Mar;3(3):225–245. doi: 10.1105/tpc.3.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Shirley B. W., Ham D. P., Senecoff J. F., Berry-Lowe S. L., Zurfluh L. L., Shah D. M., Meagher R. B. Comparison of the expression of two highly homologous members of the soybean ribulose-1,5-bisphosphate carboxylase small subunit gene family. Plant Mol Biol. 1990 Jun;14(6):909–925. doi: 10.1007/BF00019389. [DOI] [PubMed] [Google Scholar]
  15. Silverthorne J., Tobin E. M. Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell. 1990 Dec;2(12):1181–1190. doi: 10.1105/tpc.2.12.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sonnewald U., Willmitzer L. Molecular approaches to sink-source interactions. Plant Physiol. 1992 Aug;99(4):1267–1270. doi: 10.1104/pp.99.4.1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Wang J. L., Klessig D. F., Berry J. O. Regulation of C4 Gene Expression in Developing Amaranth Leaves. Plant Cell. 1992 Feb;4(2):173–184. doi: 10.1105/tpc.4.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Wanner L. A., Gruissem W. Expression dynamics of the tomato rbcS gene family during development. Plant Cell. 1991 Dec;3(12):1289–1303. doi: 10.1105/tpc.3.12.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wedding R. T. Malic enzymes of higher plants: characteristics, regulation, and physiological function. Plant Physiol. 1989 Jun;90(2):367–371. doi: 10.1104/pp.90.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Winning B. M., Bourguignon J., Leaver C. J. Plant mitochondrial NAD+-dependent malic enzyme. cDNA cloning, deduced primary structure of the 59- and 62-kDa subunits, import, gene complexity and expression analysis. J Biol Chem. 1994 Feb 18;269(7):4780–4786. [PubMed] [Google Scholar]
  22. ap Rees T., Bryce J. H., Wilson P. M., Green J. H. Role and location of NAD malic enzyme in thermogenic tissues of Araceae. Arch Biochem Biophys. 1983 Dec;227(2):511–521. doi: 10.1016/0003-9861(83)90480-0. [DOI] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES