Abstract
Immunolocalization and fluorescent in situ hybridization were used with confocal microscopy to examine patterns of photosynthetic gene expression during initial stages of leaf development in the C4 dicot Amaranthus hypochondriacus. mRNAs encoding the large and small subunit of ribulose-1,5-bisphosphate carboxylase were present in the apical dome and in all cells of the leaf primordia. In contrast, these polypeptides were detected only in cells of the ground meristem, with no accumulation detected in the apical dome or in other leaf primordia cells. The ribulose-1,5-bisphosphate carboxylase transcripts showed very little cell-type specificity as leaf structures began to differentiate, whereas their polypeptides accumulated primarily in bundle-sheath precursor cells. Phosphoenolpyruvate carboxylase and pyruvate orthophosphate dikinase mRNAs were abundant in meristems and leaf primordia, although their corresponding polypeptides did not accumulate in leaves until the leaf vascular system began to differentiate. These polypeptides were mostly restricted to premesophyll cells from their earliest detection, whereas their transcripts remained present in nearly all leaf cells. These findings indicate that individual C4 genes are independently regulated as they become initially localized to their appropriate cell types. Furthermore, posttranscriptional regulation plays a major role in determining early patterns of C4 gene expression.
Full Text
The Full Text of this article is available as a PDF (2.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- 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]
- 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]
- Boinski J. J., Wang J. L., Xu P., Hotchkiss T., Berry J. O. Post-transcriptional control of cell type-specific gene expression in bundle sheath and mesophyll chloroplasts of Amaranthus hypochondriacus. Plant Mol Biol. 1993 Jun;22(3):397–410. doi: 10.1007/BF00015971. [DOI] [PubMed] [Google Scholar]
- Fleming A. J., Mandel T., Roth I., Kuhlemeier C. The patterns of gene expression in the tomato shoot apical meristem. Plant Cell. 1993 Mar;5(3):297–309. doi: 10.1105/tpc.5.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Martineau B., Taylor W. C. Photosynthetic gene expression and cellular differentiation in developing maize leaves. Plant Physiol. 1985 Jun;78(2):399–404. doi: 10.1104/pp.78.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- Wang J. L., Long J. J., Hotchkiss T., Berry J. O. C4 Photosynthetic Gene Expression in Light- and Dark-Grown Amaranth Cotyledons. Plant Physiol. 1993 Aug;102(4):1085–1093. doi: 10.1104/pp.102.4.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]