Cell-specific Accumulation of Maize Phosphoenolpyruvate Carboxylase is Correlated with Demethylation at a Specific Site Greater Than 3 Kb Upstream of the Gene

Overview

Journal Mol Gen Genet

Specialties Genetics
Molecular Biology

Date 1991 Jan 1

PMID 2000091

Citations 29

Authors

J A Langdale

W C Taylor

T Nelson

Affiliations

Soon will be listed here.

Abstract

Development of the C4 photosynthetic pathway relies upon the cell-specific accumulation of photosynthetic enzymes. Although the molecular basis of this cell-specific gene expression is not known, regulation appears to be exerted at the level of transcript accumulation. We have investigated the relationship between gene expression patterns and DNA methylation for genes of two of the C4 photosynthetic enzymes, ribulose bisphosphate carboxylase (RuBPCase) and phosphoenolpyruvate carboxylase (PEPCase). We found no correlation between methylation state and gene expression for either the large subunit or a small subunit gene of RuBPCase. In contrast, demethylation of a specific site 5' to the PEPCase gene was correlated with the light-induced, cell-specific accumulation of PEPCase mRNA. This differentially methylated site is positioned at great distance (greater than 3 kb) from the start of transcription. This observation is made more interesting by the fact that the immediate 5' region of the gene, and some of the coding region, represents an unmethylated CpG island. Such islands are normally associated with constitutively expressed genes.

Citing Articles

C4 Phosphoenolpyruvate Carboxylase: Evolution and transcriptional regulation.

Carvalho P, Gomes C, Saibo N Genet Mol Biol. 2024; 46(3 Suppl 1):e20230190.

PMID: 38517370 PMC: 10958771. DOI: 10.1590/1678-4685-GMB-2023-0190.

Development of C4 Biochemistry and Change in Expression of Markers for Photosystems I and II in the Single-Cell C4 Species, Bienertia sinuspersici.

Yanagisawa M, Chuong S Plants (Basel). 2023; 12(1).

PMID: 36616205 PMC: 9824431. DOI: 10.3390/plants12010077.

Network and epigenetic characterization of subsets of genes specifically expressed in maize bundle sheath cells.

Tao S, Zhang W Comput Struct Biotechnol J. 2022; 20:3581-3590.

PMID: 35860403 PMC: 9287181. DOI: 10.1016/j.csbj.2022.07.004.

Targeted misexpression of NAC052, acting in H3K4 demethylation, alters leaf morphological and anatomical traits in Arabidopsis thaliana.

van Rooijen R, Schulze S, Petzsch P, Westhoff P J Exp Bot. 2019; 71(4):1434-1448.

PMID: 31740936 PMC: 7031063. DOI: 10.1093/jxb/erz509.

A Specific Transcriptome Signature for Guard Cells from the C4 Plant Gynandropsis gynandra.

Aubry S, Aresheva O, Reyna-Llorens I, Smith-Unna R, Hibberd J, Genty B Plant Physiol. 2016; 170(3):1345-57.

PMID: 26818731 PMC: 4775106. DOI: 10.1104/pp.15.01203.

References

Keshet I, Yisraeli J, Cedar H . Effect of regional DNA methylation on gene expression. Proc Natl Acad Sci U S A. 1985; 82(9):2560-4. PMC: 397603. DOI: 10.1073/pnas.82.9.2560. View

Langdale J, Rothermel B, Nelson T . Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Dev. 1988; 2(1):106-15. DOI: 10.1101/gad.2.1.106. View

Aoyagi K, Nakamoto H . Pyruvate, pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol. 1985; 78(3):661-4. PMC: 1064797. DOI: 10.1104/pp.78.3.661. View

Langdale J, Zelitch I, Miller E, Nelson T . Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J. 1988; 7(12):3643-51. PMC: 454936. DOI: 10.1002/j.1460-2075.1988.tb03245.x. View

Busslinger M, Hurst J, Flavell R . DNA methylation and the regulation of globin gene expression. Cell. 1983; 34(1):197-206. DOI: 10.1016/0092-8674(83)90150-2. View

Cedar H . DNA methylation and gene activity. Cell. 1988; 53(1):3-4. DOI: 10.1016/0092-8674(88)90479-5. View

Antequera F, Bird A . Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J. 1988; 7(8):2295-9. PMC: 457093. DOI: 10.1002/j.1460-2075.1988.tb03072.x. View

Sheen J, 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; 79(4):1072-6. PMC: 1075029. DOI: 10.1104/pp.79.4.1072. View

Sheen J . Metabolic repression of transcription in higher plants. Plant Cell. 1990; 2(10):1027-38. PMC: 159951. DOI: 10.1105/tpc.2.10.1027. View

10.

Hudspeth R, Grula J . Structure and expression of the maize gene encoding the phosphoenolpyruvate carboxylase isozyme involved in C4 photosynthesis. Plant Mol Biol. 2013; 12(5):579-89. DOI: 10.1007/BF00036971. View

11.

Bianchi M, Viotti A . DNA methylation and tissue-specific transcription of the storage protein genes of maize. Plant Mol Biol. 2013; 11(2):203-14. DOI: 10.1007/BF00015672. View

12.

Gorz A, Schafer W, Hirasawa E, Kahl G . Constitutive and light-induced DNAseI hypersensitive sites in the rbcS genes of pea (Pisum sativum). Plant Mol Biol. 2013; 11(5):561-73. DOI: 10.1007/BF00017456. View

13.

Nelson T, Langdale J . Patterns of leaf development in C4 plants. Plant Cell. 1989; 1(1):3-13. PMC: 159732. DOI: 10.1105/tpc.1.1.3. View

14.

Sheen J, 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; 5(13):3417-22. PMC: 1167374. DOI: 10.1002/j.1460-2075.1986.tb04663.x. View

15.

Ip Y, Poon D, Stone D, GRANNER D, Chalkley R . Interaction of a liver-specific factor with an enhancer 4.8 kilobases upstream of the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol. 1990; 10(7):3770-81. PMC: 360831. DOI: 10.1128/mcb.10.7.3770-3781.1990. View

16.

Gruenbaum Y, Naveh-Many T, Cedar H, Razin A . Sequence specificity of methylation in higher plant DNA. Nature. 1981; 292(5826):860-2. DOI: 10.1038/292860a0. View

17.

Bird A . CpG-rich islands and the function of DNA methylation. Nature. 1986; 321(6067):209-13. DOI: 10.1038/321209a0. View

18.

Ngernprasirtsiri J, Chollet R, Kobayashi H, Sugiyama T, Akazawa T . DNA methylation and the differential expression of C4 photosynthesis genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem. 1989; 264(14):8241-8. View

19.

Langdale J, Metzler M, Nelson T . The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. Dev Biol. 1987; 122(1):243-55. DOI: 10.1016/0012-1606(87)90349-6. View

20.

Ngernprasirtsiri J, Kobayashi H, Akazawa T . DNA methylation as a mechanism of transcriptional regulation in nonphotosynthetic plastids in plant cells. Proc Natl Acad Sci U S A. 1988; 85(13):4750-4. PMC: 280513. DOI: 10.1073/pnas.85.13.4750. View