Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1992 Feb;4(2):173–184. doi: 10.1105/tpc.4.2.173

Regulation of C4 Gene Expression in Developing Amaranth Leaves.

JL Wang 1, DF Klessig 1, JO Berry 1
PMCID: PMC160118  PMID: 12297645

Abstract

Immunofluorescence microscopy and in situ hybridization were used to examine the expression of genes encoding C4 photosynthetic enzymes during early leaf development in the C4 dicotyledonous grain plant amaranth. During early developmental stages, the chloroplast-encoded large subunit and nuclear-encoded small subunit genes of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCase) were expressed in both bundle sheath and mesophyll cells in a C3-type pattern. The RuBPCase proteins and mRNAs became specifically localized to bundle sheath cells in the characteristic C4-type pattern as the leaves continued to expand and develop. Changes in the localization of the RuBPCase proteins corresponded closely with changes in the localization of their mRNAs, indicating that the cell-specific expression of genes encoding RuBPCase is controlled, at least in part, at the level of transcript accumulation. Genes encoding pyruvate orthophosphate dikinase were expressed specifically in mesophyll cells at all developmental stages examined. Immunolocalization with antibodies raised against phosphoenolpyruvate carboxylase (PEPCase) showed that this enzyme is present only in leaf mesophyll cells, even though RNA sequences with homology to PEPCase gene sequences were present in both bundle sheath and mesophyll cells. These results suggest that the regulation of genes encoding PEPCase in amaranth is complex and could involve the differential expression of divergent PEPCase genes or possibly regulation at the post-transcriptional level.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

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

  1. Aoyagi K., Nakamoto H. Pyruvate, pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol. 1985 Jul;78(3):661–664. doi: 10.1104/pp.78.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Berry J. O., Carr J. P., Klessig D. F. mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4190–4194. doi: 10.1073/pnas.85.12.4190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Ferreira R. B., Davies D. D. Protein degradation in lemna with particular reference to ribulose bisphosphate carboxylase: I. The effect of light and dark. Plant Physiol. 1987 Apr;83(4):869–877. doi: 10.1104/pp.83.4.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hatch M. D. Regulation of enzymes in C4 photosynthesis. Curr Top Cell Regul. 1978;14:1–27. [PubMed] [Google Scholar]
  7. 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]
  8. Langdale J. A., Nelson T. Spatial regulation of photosynthetic development in C4 plants. Trends Genet. 1991 Jun;7(6):191–196. doi: 10.1016/0168-9525(91)90435-s. [DOI] [PubMed] [Google Scholar]
  9. Langdale J. A., Rothermel B. A., Nelson T. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Dev. 1988 Jan;2(1):106–115. doi: 10.1101/gad.2.1.106. [DOI] [PubMed] [Google Scholar]
  10. Langdale J. A., Taylor W. C., Nelson T. Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site greater than 3 kb upstream of the gene. Mol Gen Genet. 1991 Jan;225(1):49–55. doi: 10.1007/BF00282641. [DOI] [PubMed] [Google Scholar]
  11. Langdale J. A., Zelitch I., Miller E., Nelson T. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J. 1988 Dec 1;7(12):3643–3651. doi: 10.1002/j.1460-2075.1988.tb03245.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Matsuoka M., Ozeki Y., Yamamoto N., Hirano H., Kano-Murakami Y., Tanaka Y. Primary structure of maize pyruvate, orthophosphate dikinase as deduced from cDNA sequence. J Biol Chem. 1988 Aug 15;263(23):11080–11083. [PubMed] [Google Scholar]
  13. Michalowski C. B., Bohnert H. J., Klessig D. F., Berry J. O. Nucleotide sequence of rbcL from Amaranthus hypochondriacus chloroplasts. Nucleic Acids Res. 1990 Apr 25;18(8):2187–2187. doi: 10.1093/nar/18.8.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nelson T., Langdale J. A. Patterns of leaf development in C4 plants. Plant Cell. 1989 Jan;1(1):3–13. doi: 10.1105/tpc.1.1.3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nikolau B. J., Klessig D. F. Coordinate, Organ-Specific and Developmental Regulation of Ribulose 1,5-Bisphosphate Carboxylase Gene Expression in Amaranthus hypochondriacus. Plant Physiol. 1987 Sep;85(1):167–173. doi: 10.1104/pp.85.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rickers J., Cushman J. C., Michalowski C. B., Schmitt J. M., Bohnert H. J. Expression of the CAM-form of phospho(enol)pyruvate carboxylase and nucleotide sequence of a full length cDNA from Mesembryanthemum crystallinum. Mol Gen Genet. 1989 Feb;215(3):447–454. doi: 10.1007/BF00427042. [DOI] [PubMed] [Google Scholar]
  17. Schuster G., Ohad I., Martineau B., Taylor W. C. Differentiation and development of bundle sheath and mesophyll thylakoids in maize. Thylakoid polypeptide composition, phosphorylation, and organization of photosystem II. J Biol Chem. 1985 Sep 25;260(21):11866–11873. [PubMed] [Google Scholar]
  18. 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]
  19. Sheen J. Y., Bogorad L. Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem. 1987 Aug 25;262(24):11726–11730. [PubMed] [Google Scholar]
  20. Sheen J. Y., Bogorad L. Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiol. 1985 Dec;79(4):1072–1076. doi: 10.1104/pp.79.4.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sheen J. Y., Bogorad L. Expression of the ribulose-1,5-bisphosphate carboxylase large subunit gene and three small subunit genes in two cell types of maize leaves. EMBO J. 1986 Dec 20;5(13):3417–3422. doi: 10.1002/j.1460-2075.1986.tb04663.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]

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

RESOURCES