Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1993 Aug;102(4):1085–1093. doi: 10.1104/pp.102.4.1085

C4 Photosynthetic Gene Expression in Light- and Dark-Grown Amaranth Cotyledons.

J L Wang 1, J J Long 1, T Hotchkiss 1, J O Berry 1
PMCID: PMC158893  PMID: 12231890

Abstract

The patterns of expression for genes encoding several C4 photosynthetic enzymes were examined in light-grown and dark-grown (etiolated) cotyledons of amaranth (Amaranthus hypochondriacus), a dicotyledonous C4 plant. The large subunit and small subunit of ribulose-1,5-bisphosphate carboxylase (RuBPCase), phosphoenolpyruvate carboxylase (PEPCase), and pyruvate orthophosphate dikinase (PPdK) were all present in the cotyledons by d 2 after planting when the seedlings first emerged from the seed coat. Kranz anatomy was apparent in light-grown cotyledons throughout development, and the overall patterns of C4 gene expression were similar to those recently described for developing amaranth leaves (J.L. Wang, D.F. Klessig, J.O. Berry [1992] Plant Cell 4: 173-184). RuBPCase mRNA and proteins were present in both bundle sheath and mesophyll cells in a C3-like pattern during early development and became progressively more localized to bundle sheath cells in the C4-type pattern as the cotyledons expanded over 2 to 7 d. PEPCase and PPdK polypeptides were localized to mesophyll cells throughout development, even though PEPCase transcripts were detected in both bundle sheath and mesophyll cells. Kranz anatomy also developed in cotyledons grown in complete darkness. In 7-d-old dark-grown cotyledons, RuBPCase, PPdK, and PEPCase were all localized to the appropriate cell types, although at somewhat lower levels than in light-grown cotyledons. These findings demonstrate that the leaves and postembryonic cotyledons of amaranth undergo common developmental programs of C4 gene expression during maturation. Furthermore, light is not required for the cell-type-specific expression of genes encoding RuBPCase and other photosynthetic enzymes in this dicotyledonous C4 plant.

Full Text

The Full Text of this article is available as a PDF (2.9 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., 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]
  3. 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]
  4. 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]
  5. Hatch M. D. Regulation of enzymes in C4 photosynthesis. Curr Top Cell Regul. 1978;14:1–27. [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Meinke D. W. A Homoeotic Mutant of Arabidopsis thaliana with Leafy Cotyledons. Science. 1992 Dec 4;258(5088):1647–1650. doi: 10.1126/science.258.5088.1647. [DOI] [PubMed] [Google Scholar]
  10. Miziorko H. M., Lorimer G. H. Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem. 1983;52:507–535. doi: 10.1146/annurev.bi.52.070183.002451. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. 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]

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

RESOURCES