Abstract
In plant genomes, there exist discrete regions rich in CpG dinucleotides, namely CpG clusters. In rice, most of these CpG clusters are associated with genes. Rice genes are grouped into one of the five classes according to the position of an associated CpG cluster. Among them, class 1 genes, which harbor a CpG cluster at the 5′-terminus, share similarities with human genes having CpG islands. In the present study, by analyzing plant genome sequence data, primarily from rice, we investigated the chromosomal distribution of genes of each class, mainly class 1 genes. Class 1 genes were not uniformly distributed across the rice genome, but were clustered into discrete chromosomal segments. EST-based analysis of the distribution of expressed genes indicates that this segmental distribution of class 1 genes caused a preferential distribution of expressed genes within class 1 gene-rich segments. We then compared the methylation status of genes of each class to examine the possibility that differential DNA methylation, if any, is relevant to the observed differential expression level of genes inside and outside the class 1 segments. The difference in the methylation level between these genes was revealed to be fairly small, which does not support the above-mentioned possibility.
Similar content being viewed by others
References
Antequera F, Bird AP (1988) Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J 7:2295–2299
Ashikawa I (2001) Gene-associated CpG islands in plants as revealed by analysis of genomic sequences. Plant J 26:617–625
Ashikawa I (2002) Gene-associated CpG islands and the expression pattern of genes in rice. DNA Res 9:131–134
Bennetzen JL, Chrick K, Springer PS, Brown WE, SanMiguel P (1994) Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37:565–576
Bird AP (1987) CpG islands as gene markers in vertebrate nucleus. Trends Genet 3:342–347
Bird AP (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21
Bird AP, Taggart M, Frommer M, Miller OJ, Macleod D (1985) A fraction of the mouse genome that is derived from islands of nonmethylated CpG-rich DNA. Cell 40:91–99
Cross SH, Bird AP (1995) CpG islands and genes. Curr Opin Genet Dev 5:309–314
Dunham I, Shimizu N, Roe BA et al. (1999) The DNA sequence of human chromosome 22. Nature 402:489–495
Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10:217–223
Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8:967–974
Gardiner-Garden M, Frommer M (1987) CpG islands in vertebrate genomes. J Mol Biol 196:261–282
Gardiner-Garden M, Frommer M (1992) Significant CpG-rich regions in angiosperm genes. J Mol Evol 34:231–245
Gruenbaum Y, Naveh-Many T, Ceder H, Razin A (1981) Sequence specificity of methylation in higher plant DNA. Nature 292:860–862
Hashimshony T, Zhang J, Keshet I, Bustin M, Ceder H (2003) The role of DNA methylation in setting up chromatin structure during development. Nat Genet 34:187–192
Hattori M, Fujiyama A, Taylor TD et al (2000) The DNA sequence of human chromosome 21. Nature 405:311–319
Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277:1100–1103
Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H et al (2003) Collection, mapping, and annotation of over 28000 cDNA clones from japonica rice. Science 301:376–379
Langdale JA, Taylor WC, Nelson T (1991) Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site >3 kb upstream of the gene. Mol Gen Genet 225:49–55
Larsen F, Gundersen G, Lopez R, Prydz H (1992) CpG islands as gene markers in the human genome. Genomics 13:1095–1107
Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16:753–770
Moore G, Abbo S, Cheung W et al (1993) Key features of cereal genome organization as revealed by the use of cytosine methylation-sensitive restriction endonucleases. Genomics 15:472–482
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Panstruga R, Buschges R, Piffanelli P, Schulze-Lefert P (1998) A contiguous 60 kb genomic stretch from barley reveals molecular evidence for gene islands in a monocot genome. Nucleic Acids Res 26:1056–1062
Rabinowicz PD, Palmer LE, May BP, Hemann MT, Lowe SW, McCombie WR, Martienssen RA (2003) Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res 13:2658–2664
Rombauts S, Florquin K, Lescot M, Marchal K, Rouze P, Van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132:1162–1176
Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T et al (2002) RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102
Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y et al (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145
Sorensen MB, Muller M, Skerritt J, Simpson D (1996) Hordein promoter methylation and transcriptional activity in wild-type and mutant barley endosperm. Mol Gen Genet 250:750–760
Turcotte K, Srinivasan S, Bureau T (2001) Survey of transposable elements from rice genomic sequences. Plant J 25:169–179
Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J et al (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535
Acknowledgements
We thank K. Higo for his encouragement during this work. This study was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Rice Genome Project SY-1101).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. McCombie
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Ashikawa, I., Numa, H. & Sakata, K. Segmental distribution of genes harboring a CpG island-like region on rice chromosomes. Mol Genet Genomics 275, 18–25 (2006). https://doi.org/10.1007/s00438-005-0060-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-005-0060-1