Light-regulated and cell-specific methylation of the maize PEPC promoter

Journal of Experimental Botany

Volumn 63, Issue 3, 2012, Pages 1381-1390

  Tolley, Ben J ^a   Woodfield, Helen ^a   Wanchana, Samart ^b   Bruskiewich, Richard ^b   Hibberd, Julian M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

Bundle sheath; C 4 photosynthesis; maize; mesophyll; methylation; PEPC

Indexed keywords

PHOSPHOENOLPYRUVATE CARBOXYLASE;

ARTICLE; DNA METHYLATION; ENZYMOLOGY; GENETICS; MAIZE; PROMOTER REGION;

DNA METHYLATION; PHOSPHOENOLPYRUVATE CARBOXYLASE; PROMOTER REGIONS, GENETIC; ZEA MAYS;

ZEA MAYS;

EID: 84856896946     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err367     Document Type: Article

References (56)

1. Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M, Westhoff P. 2007. Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. The Plant Cell 19, 3391-3402.
2. Astier Y, Braha O, Bayley H. 2006. Toward single molecule DNA sequencing: direct identification of ribonucleoside and deoxyribonucleoside 5'-monophosphates by using an engineered protein nanopore equipped with a molecular adapter. Journal of the American Chemical Society 128, 1705-1710.
3. Bader S, Walker M, McQueen HA, Sellar R, Oei E, Wopereis S, Zhu Y, Peter A, Bird AP, Harrison DJ. 2003. MBD1, MBD2, and CGBP genes at chromosome 18q21 are infrequently mutated in human colon and lung cancers. Oncogene 22, 3506-3510.
4. Baubec T, Pecinka A, Rozhon W, Scheid OM. 2009. Effective, homogeneous and transient interference with cytosine methylation in plant genomic DNA by zebularine. The Plant Journal 57, 542-554.
5. Bianchi MW, Viotti A. 1988. DNA Methylation and tissue-specific transcription of the storage protein genes of maize. Plant Molecular Biology 11, 203-214.
6. Blackledge NP, Zhou JC, Tolstorukov MY, Farcas AM, Park PJ, Klose RJ. 2010. CpG islands recruit a histone H3 lysine 36 demethylase. Molecular Cell 38, 179-190.
7. Brown NJ, Newell CA, Stanley S, Chen JE, Perrin AJ, Kajala K, Hibberd JM. 2011. Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331, 1436-1439.
8. Brown NJ, Parsley K, Hibberd JM. 2005. The future of C4 research: maize, Flaveria orCleome? Trends in Plant Science 10, 215-221.
9. Bucherna N, Szabo E, Heszky LS, Nagy I. 2001. DNA methylation and gene expression differences during alternative in vitro morphogenic processes in eggplant (Solanum melongena L.). In vitro Cellular and Developmental Biology-Plant 37, 672-677.
10. Cedar H. 1988. DNA methylation and gene activity. Cell 53, 3-4.
11. Chollet R, Vidal J, O'Leary MH. 1996. Phospho enolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 273-298.
12. Christman JK. 2002. 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 21, 5483-5495.
13. Clarke J, Wu HC, Jayasinghe L, Patel A, Reid A, Bayley H. 2009. Continuous base identification for single-molecule nanopore DNA sequencing. Nature Nanotechnology 4, 265-270.
14. Danker T, Dreesen B, Offermann S, Horst I, Peterhaensel C. 2008. Developmental information but not promoter activity controls the methylation state of histone H3 lysine 4 on two photosynthetic genes in maize. The Plant Journal 53, 465-474.
15. Fleige S, Pfaffl MW. 2006. RNA integrity and the effect on the realtime qRT-PCR performance. Molecular Aspects of Medicine 27, 126-139.
16. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proceedings of the National Academy of Sciences, USA 89, 1827-1831.
17. Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P. 2004. cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phospho enolpyruvate carboxylase gene. The Plant Cell 16, 1077-1090.
18. Henderson IR, Chan SR, Cao X, Johnson L, Jacobsen SE. 2010. Accurate sodium bisulfite sequencing in plants. Epigenetics 5, 47-49.
19. Hepburn AG, Belanger FC, Mattheis JR. 1987. DNA methylation in plants. Developmental Genetics 8, 475-493.
20. Hibberd JM, Covshoff S. 2010. The regulation of gene expression required for C4 photosynthesis. Annual Review of Plant Biology 61, 181-207.
21. Huang N-C, Li C-H, Lee J-Y, Yen HE. 2010. Cytosine methylation changes in the ice plant Ppc1 promoter during transition from C3 to Crassulacean acid metabolism. Plant Science 178, 41-46.
22. Jones PA. 1985. Altering gene expression with 5-azacytidine. Cell 40, 485-486.
23. Kano-Murakami Y, Suzuki I, Sugiyama T, Matsuoka M. 1991. Sequence-specific interactions of a maize factor with a GC-rich repeat in the phosphoenolpyruvate carboxylase gene. Molecular and General Genetics 225, 203-208.
24. Kasianowicz JJ, Brandin E, Branton D, Deamer DW. 1996. Characterization of individual polynucleotide molecules using a membrane channel. Proceedings of the National Academy of Sciences, USA 93, 13770-13773.
25. Kausch AP, Owen TP, Zachwieja SJ, Flynn AR, Sheen J. 2001. Mesophyll-specific, light and metabolic regulation of the C4 PPCZm1 promoter in transgenic maize. Plant Molecular Biology 45,1-15.
26. Ku MSB, Agarie S, Nomura M, etal. 1999. High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nature Biotechnology 17, 76-80.
27. Lande-Diner L, Zhang J, Ben-Porath I, Amariglio N, Keshet I, Hecht M, Azuara V, Fisher AG, Rechavi G, Cedar H. 2007. Role of DNA methylation in stable gene repression. Journal of Biological Chemistry 282, 12194-12200.
28. Langdale JA, Metzler MC, Nelson T. 1987. The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. Developmental Biology 122, 243-255.
29. Langdale JA, Rothermel BA, Nelson T. 1988. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes and Development 2, 106-115.
30. Langdale JA, Taylor WC, Nelson T. 1991. Cell-specific accumulation of maize phospho enolpyruvate carboxylase is correlated with demethylation at a specific site >3 kb upstream of the gene. Molecular and General Genetics 225, 49-55.
31. Li L-C, Dahiya R. 2002. MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431.
32. Lin C, Shen B, Xu Z, Kollner TG, Degenhardt J, Dooner HK. 2008. Characterization of the monoterpene synthase gene tps26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiology 146, 940-951.
33. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2~AA CT method. Methods 25, 402-408.
34. Lucchini R, Sogo JM. 1995. Replication of transcriptionally active chromatin. Nature 374, 276-280.
35. Markelz NH, Costich DE, Brutnell TP. 2003. Photomorphogenic responses in maize seedling development. Plant Physiology 133, 1578-1591.
36. Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano-Murakami Y. 1993. Expression of a rice homeobox gene causes altered morphology of transgenic plants. The Plant Cell 5,1039-1048.
37. Matsuoka M, Kyozuka J, Shimamoto K, Kano-Murakami Y. 1994. The promoters of two carboxylases in a C4 plant (maize) direct cell-specific, light-regulated expression in a C3 plant (rice). The Plant Journal 6, 311-319.
38. Nick H, Bowen B, Ferl RJ, Gilbert W. 1986. Detection of cytosine methylation in the maize alcohol dehydrogenase gene by genomic sequencing. Nature 319, 243-246.
39. Nomura M, Sentoku N, Nishimura A, et al. 2000. The evolution of C4 plants: acquisition of cis-regulatory sequences in the promoter of C4-type pyruvate, orthophosphate dikinase gene. The Plant Journal 22, 211-221.
40. Offermann S, Danker T, Dreymü ller D, Kalamajka R, Tö psch S, Weyand K, Peterhänsel C. 2006. Illumination is necessary and sufficient to induce histone acetylation independent of transcriptional activity at the C4-specific phosphoenolpyruvate carboxylase promoter in maize. Plant Physiology 141, 1078-1088.
41. Okimoto R, Sachs MM, Porter EK, Freeling M. 1980. Patterns of polypeptide synthesis in various maize organs under anaerobiosis. Planta 150, 89-94.
42. Sawers RJ, Liu P, Anufrikova K, Hwang JT, Brutnell TP. 2007. A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8, 12.
43. Schä ffner AR, Sheen J-Y. 1992. Maize C4 photosynthesis involves differential regulation of phosphoenol pyruvate carboxylase genes. The Plant Journal 2, 221-232.
44. Spena A, Viotti A, Pirotta V. 1983. Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. Journal of Molecular Biology 169, 799-811.
45. Stockhaus J, Schlue U, Koczor M, Chitty JA, Taylor WC, Westhoff P. 1997. The promoter of the gene encoding the C4 form of phospho enolpyruvate carboxylase directs mesophyll-specific expression in transgenic C4 Flaveria spp. The Plant Cell 9, 479-89.
46. Suzuki MM, Bird A. 2008. DNA methylation landscapes: provocative insights from epigenomics. Nature Reviews Genetics 9, 465-476.
47. Taniguchi M, Izawa K, Ku MSB, Lin JH, Saito H, Ishida Y, Ohta S, Komari T, Matsuoka M, Sugiyama T. 2000. Binding of cell type-specific nuclear proteins to the 5#-flanking region of maize C4 phospho enolpyruvate carboxylase gene confers its differential transcription in mesophyll cells. Plant Molecular Biology 44, 543-57.
48. Thomson JP, Skene PJ, Selfridge J, et al. 2010. CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464, 1082-1086.
49. Voo KS, Carlone DL, Jacobsen BM, Flodin A, Skalnik DG. 2000. Cloning of a mammalian transcriptional activator that binds unmethylated CpG motifs and shares a CXXC domain with DNA methyltransferase, human trithorax, and methyl-CpG binding domain protein 1. Molecular Cell Biology 20, 2108-2121.
50. Wang RYH, Gehrke CW, Ehrlich M. 1980. Comparison of bisulphite modification of 5-methyldeoxycytidine and deoxycytidine residues. Nucleic Acids Research 8, 4777-4790.
51. Weber M, Schubeler D. 2007. Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Current Opinion in Cell Biology 19, 273-280.
52. Yanagisawa S. 1995. A novel DNA-binding domain that may form a single zinc finger motif. Nucleic Acids Research 23, 3403-3410.
53. Yanagisawa S, Izui K. 1990. Multiple interactions between tissue-specific nuclear proteins and the promoter of the phosphoenol pyruvate carboxylase gene for C4 photosynthesis in Zea mays. Molecular and General Genetics 224, 325-332.
54. Yanagisawa S, Izui K. 1992. MNF1, a leaf tissue-specific DNA-binding protein of maize, interacts with the cauliflower mosaic virus 35S promoter as well as the C4 photosynthetic phosphoenol pyruvate carboxylase gene promoter. Plant Molecular Biology 19, 545-553.
55. Yanagisawa S, Izui K. 1993. Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. Journal of Biological Chemistry 268, 16028-16036.
56. Yanagisawa S, Sheen J-Y. 1998. Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. The Plant Cell 10, 75-89.