Abstract
Different sets of genes for photosynthesis are expressed in mesophyll cells (MCs) and bundle sheath cells (BSCs)--the two adjacent but morphologically and functionally distinct types of photosynthetic cells in leaves of maize and other C4 plants. For example, light-harvesting chlorophyll a/b-binding proteins of photosystem II, which are encoded by a family of cab genes, are 3- to 4-fold more abundant in maize MCs than in BSCs. Each maize cab gene is different from the others in its relative expression in MCs vs. BSCs and in its degree of photoresponsiveness. The gene cab-m1 is positively photoregulated and is highly preferentially expressed in MCs. A 159-bp sequence in the 5' flanking region of this gene (-1026 to -868 relative to the translation start site) is required for MC-preferred expression of a reporter gene in greening maize leaves. Deletion as well as gain-of-function experiments have now shown that all of the sequence information required for MC-preferred expression resides within this mesophyll-specifying region and that cab-m1 is preferentially expressed in MCs because of the presence of two types of sequence elements: one is required for suppressing expression in BSCs and the other for promoting expression in MCs. One of the four cis-acting regions mapped within the mesophyll-specifying region resembles the AT-1 box of some plant gene negative regulatory elements. Various combinations of such MC-specific enhancing and BSC-specific repressing regions could make maize cab gene family members different from one another in their relative expression in MCs vs. BSCs.
Full text
PDF
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bansal K. C., Viret J. F., Haley J., Khan B. M., Schantz R., Bogorad L. Transient expression from cab-m1 and rbcS-m3 promoter sequences is different in mesophyll and bundle sheath cells in maize leaves. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3654–3658. doi: 10.1073/pnas.89.8.3654. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Becker T. W., Templeman T. S., Viret J. F., Bogorad L. The cab-m7 gene: a light-inducible, mesophyll-specific gene of maize. Plant Mol Biol. 1992 Oct;20(1):49–60. doi: 10.1007/BF00029148. [DOI] [PubMed] [Google Scholar]
- Bevan M., Barnes W. M., Chilton M. D. Structure and transcription of the nopaline synthase gene region of T-DNA. Nucleic Acids Res. 1983 Jan 25;11(2):369–385. doi: 10.1093/nar/11.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Castresana C., Garcia-Luque I., Alonso E., Malik V. S., Cashmore A. R. Both positive and negative regulatory elements mediate expression of a photoregulated CAB gene from Nicotiana plumbaginifolia. EMBO J. 1988 Jul;7(7):1929–1936. doi: 10.1002/j.1460-2075.1988.tb03030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Datta N., Cashmore A. R. Binding of a pea nuclear protein to promoters of certain photoregulated genes is modulated by phosphorylation. Plant Cell. 1989 Nov;1(11):1069–1077. doi: 10.1105/tpc.1.11.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kano-Murakami Y., Suzuki I., Sugiyama T., Matsuoka M. Sequence-specific interactions of a maize factor with a GC-rich repeat in the phosphoenolpyruvate carboxylase gene. Mol Gen Genet. 1991 Feb;225(2):203–208. doi: 10.1007/BF00269849. [DOI] [PubMed] [Google Scholar]
- Langdale J. A., Lane B., Freeling M., Nelson T. Cell lineage analysis of maize bundle sheath and mesophyll cells. Dev Biol. 1989 May;133(1):128–139. doi: 10.1016/0012-1606(89)90304-7. [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]
- Link G., Coen D. M., Bogorad L. Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell. 1978 Nov;15(3):725–731. doi: 10.1016/0092-8674(78)90258-1. [DOI] [PubMed] [Google Scholar]
- Luan S., Bogorad L. A rice cab gene promoter contains separate cis-acting elements that regulate expression in dicot and monocot plants. Plant Cell. 1992 Aug;4(8):971–981. doi: 10.1105/tpc.4.8.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsuoka M., Numazawa T. Cis-acting elements in the pyruvate, orthophosphate dikinase gene from maize. Mol Gen Genet. 1991 Aug;228(1-2):143–152. doi: 10.1007/BF00282459. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarkar G., Sommer S. S. The "megaprimer" method of site-directed mutagenesis. Biotechniques. 1990 Apr;8(4):404–407. [PubMed] [Google Scholar]
- 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]
- Sheen J. Y., Bogorad L. Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7811–7815. doi: 10.1073/pnas.83.20.7811. [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]