Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1990 Apr 11;18(7):1859–1867. doi: 10.1093/nar/18.7.1859

Gene distribution and isochore organization in the nuclear genome of plants.

L M Montero 1, J Salinas 1, G Matassi 1, G Bernardi 1
PMCID: PMC330607  PMID: 2336360

Abstract

The genomic distribution of 23 nuclear genes from three dicotyledons (pea, sunflower, tobacco) and five monocotyledons of the Gramineae family (barley, maize, rice, oat, wheat) was studied by localizing these genes in DNA fractions obtained by preparative centrifugation in Cs2SO4/BAMD density gradients. Each one of these genes (and of many other related genes and pseudogenes) was found to be located in DNA fragments (50-100 Kb in size) that were less than 1-2% GC apart from each other. This definitively demonstrates the existence of isochores in plant genomes, namely of compositionally homogeneous DNA regions at least 100-200 Kb in size. Moreover, the GC levels of the 23 coding sequences studied, of their first, second and third codon positions, and of the corresponding introns were found to be linearly correlated with the GC levels of the isochores harboring those genes. Compositional correlations displayed increasing slopes when going from second to first to third codon position with obvious effects on codon usage. Coding sequences for seed storage proteins and phytochrome of Gramineae deviate from the compositional correlations just described. Finally, CpG doublets of coding sequences were characterized by a shortage that decreased and vanished with increasing GC levels of the sequences. A number of these findings bear a striking similarity with results previously obtained for vertebrate genes.

Full text

PDF
1859

Images in this article

1862Image
on p.1862
1862Image
on p.1862
1863Image
on p.1863

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antequera F., Bird A. P. Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J. 1988 Aug;7(8):2295–2299. doi: 10.1002/j.1460-2075.1988.tb03072.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baulcombe D C, Huttly A K, Martienssen R A, Barker R F, Jarvis M G. A novel wheat alpha-amylase gene (alpha-Amy3). Mol Gen Genet. 1987 Aug;209(1):33–40. doi: 10.1007/BF00329833. [DOI] [PubMed] [Google Scholar]
  3. Bennetzen J. L., Swanson J., Taylor W. C., Freeling M. DNA insertion in the first intron of maize Adh1 affects message levels: cloning of progenitor and mutant Adh1 alleles. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4125–4128. doi: 10.1073/pnas.81.13.4125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernardi G., Bernardi G. Compositional constraints and genome evolution. J Mol Evol. 1986;24(1-2):1–11. doi: 10.1007/BF02099946. [DOI] [PubMed] [Google Scholar]
  5. Bernardi G., Mouchiroud D., Gautier C., Bernardi G. Compositional patterns in vertebrate genomes: conservation and change in evolution. J Mol Evol. 1988 Dec;28(1-2):7–18. doi: 10.1007/BF02143493. [DOI] [PubMed] [Google Scholar]
  6. Bernardi G., Olofsson B., Filipski J., Zerial M., Salinas J., Cuny G., Meunier-Rotival M., Rodier F. The mosaic genome of warm-blooded vertebrates. Science. 1985 May 24;228(4702):953–958. doi: 10.1126/science.4001930. [DOI] [PubMed] [Google Scholar]
  7. Bernardi G. The isochore organization of the human genome. Annu Rev Genet. 1989;23:637–661. doi: 10.1146/annurev.ge.23.120189.003225. [DOI] [PubMed] [Google Scholar]
  8. Broglie R., Bellemare G., Bartlett S. G., Chua N. H., Cashmore A. R. Cloned DNA sequences complementary to mRNAs encoding precursors to the small subunit of ribulose-1,5-bisphosphate carboxylase and a chlorophyll a/b binding polypeptide. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7304–7308. doi: 10.1073/pnas.78.12.7304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cashmore A. R. Structure and expression of a pea nuclear gene encoding a chlorophyll a/b-binding polypeptide. Proc Natl Acad Sci U S A. 1984 May;81(10):2960–2964. doi: 10.1073/pnas.81.10.2960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coruzzi G., Broglie R., Edwards C., Chua N. H. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J. 1984 Aug;3(8):1671–1679. doi: 10.1002/j.1460-2075.1984.tb02031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dennis E. S., Gerlach W. L., Pryor A. J., Bennetzen J. L., Inglis A., Llewellyn D., Sachs M. M., Ferl R. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 1984 May 11;12(9):3983–4000. doi: 10.1093/nar/12.9.3983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Forde B. G., Heyworth A., Pywell J., Kreis M. Nucleotide sequence of a B1 hordein gene and the identification of possible upstream regulatory elements in endosperm storage protein genes from barley, wheat and maize. Nucleic Acids Res. 1985 Oct 25;13(20):7327–7339. doi: 10.1093/nar/13.20.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gebhardt C., Oliver J. E., Forde B. G., Saarelainen R., Miflin B. J. Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J. 1986 Jul;5(7):1429–1435. doi: 10.1002/j.1460-2075.1986.tb04379.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gouy M., Milleret F., Mugnier C., Jacobzone M., Gautier C. ACNUC: a nucleic acid sequence data base and analysis system. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):121–127. doi: 10.1093/nar/12.1part1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gruenbaum Y., Naveh-Many T., Cedar H., Razin A. Sequence specificity of methylation in higher plant DNA. Nature. 1981 Aug 27;292(5826):860–862. doi: 10.1038/292860a0. [DOI] [PubMed] [Google Scholar]
  16. Hershey H. P., Barker R. F., Idler K. B., Lissemore J. L., Quail P. H. Analysis of cloned cDNA and genomic sequences for phytochrome: complete amino acid sequences for two gene products expressed in etiolated Avena. Nucleic Acids Res. 1985 Dec 9;13(23):8543–8559. doi: 10.1093/nar/13.23.8543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hershey H. P., Colbert J. T., Lissemore J. L., Barker R. F., Quail P. H. Molecular cloning of cDNA for Avena phytochrome. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2332–2336. doi: 10.1073/pnas.81.8.2332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hudspeth R. L., Glackin C. A., Bonner J., Grula J. W. Genomic and cDNA clones for maize phosphoenolpyruvate carboxylase and pyruvate,orthophosphate dikinase: Expression of different gene-family members in leaves and roots. Proc Natl Acad Sci U S A. 1986 May;83(9):2884–2888. doi: 10.1073/pnas.83.9.2884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Izui K., Ishijima S., Yamaguchi Y., Katagiri F., Murata T., Shigesada K., Sugiyama T., Katsuki H. Cloning and sequence analysis of cDNA encoding active phosphoenolpyruvate carboxylase of the C4-pathway from maize. Nucleic Acids Res. 1986 Feb 25;14(4):1615–1628. doi: 10.1093/nar/14.4.1615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kemp J. D., Sutton D. W. A chemical and physical method for determining the complete base composition of plant DNA. Biochim Biophys Acta. 1976 Mar 4;425(2):148–156. doi: 10.1016/0005-2787(76)90020-4. [DOI] [PubMed] [Google Scholar]
  21. Kridl J. C., Vieira J., Rubenstein I., Messing J. Nucleotide sequence analysis of a zein genomic clone with a short open reading frame. Gene. 1984 Apr;28(1):113–118. doi: 10.1016/0378-1119(84)90093-3. [DOI] [PubMed] [Google Scholar]
  22. Lamppa G. K., Morelli G., Chua N. H. Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol Cell Biol. 1985 Jun;5(6):1370–1378. doi: 10.1128/mcb.5.6.1370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lebrun M., Waksman G., Freyssinet G. Nucleotide sequence of a gene encoding corn ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (rbcs). Nucleic Acids Res. 1987 May 26;15(10):4360–4360. doi: 10.1093/nar/15.10.4360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Llewellyn D. J., Finnegan E. J., Ellis J. G., Dennis E. S., Peacock W. J. Structure and expression of an alcohol dehydrogenase 1 gene from Pisum sativum (cv. "Greenfeast"). J Mol Biol. 1987 May 5;195(1):115–123. doi: 10.1016/0022-2836(87)90331-7. [DOI] [PubMed] [Google Scholar]
  25. Lycett G. W., Croy R. R., Shirsat A. H., Boulter D. The complete nucleotide sequence of a legumin gene from pea (Pisum sativum L.). Nucleic Acids Res. 1984 Jun 11;12(11):4493–4506. doi: 10.1093/nar/12.11.4493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matassi G., Montero L. M., Salinas J., Bernardi G. The isochore organization and the compositional distribution of homologous coding sequences in the nuclear genome of plants. Nucleic Acids Res. 1989 Jul 11;17(13):5273–5290. doi: 10.1093/nar/17.13.5273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mazur B. J., Chui C. F. Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco. Nucleic Acids Res. 1985 Apr 11;13(7):2373–2386. doi: 10.1093/nar/13.7.2373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Okita T. W., Cheesbrough V., Reeves C. D. Evolution and heterogeneity of the alpha-/beta-type and gamma-type gliadin DNA sequences. J Biol Chem. 1985 Jul 5;260(13):8203–8213. [PubMed] [Google Scholar]
  29. Philipps G., Chaubet N., Chaboute M. E., Ehling M., Gigot C. Genomic organization and nucleotide sequences of two corn histone H4 genes. Gene. 1986;42(2):225–229. doi: 10.1016/0378-1119(86)90301-x. [DOI] [PubMed] [Google Scholar]
  30. Pintor-Toro J. A., Langridge P., Feix G. Isolation and characterization of maize genes coding for zein proteins of the 21000 dalton size class. Nucleic Acids Res. 1982 Jul 10;10(13):3845–3860. doi: 10.1093/nar/10.13.3845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Salinas J., Matassi G., Montero L. M., Bernardi G. Compositional compartmentalization and compositional patterns in the nuclear genomes of plants. Nucleic Acids Res. 1988 May 25;16(10):4269–4285. doi: 10.1093/nar/16.10.4269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schwarz-Sommer Z., Gierl A., Klösgen R. B., Wienand U., Peterson P. A., Saedler H. The Spm (En) transposable element controls the excision of a 2-kb DNA insert at the wx allele of Zea mays. EMBO J. 1984 May;3(5):1021–1028. doi: 10.1002/j.1460-2075.1984.tb01922.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Tingey S. V., Walker E. L., Coruzzi G. M. Glutamine synthetase genes of pea encode distinct polypeptides which are differentially expressed in leaves, roots and nodules. EMBO J. 1987 Jan;6(1):1–9. doi: 10.1002/j.1460-2075.1987.tb04710.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wagner I., Capesius I. Determination of 5-methylcytosine from plant DNA by high-performance liquid chromatography. Biochim Biophys Acta. 1981 Jun 26;654(1):52–56. doi: 10.1016/0005-2787(81)90135-0. [DOI] [PubMed] [Google Scholar]
  36. Waksman G., Freyssinet G. Nucleotide sequence of a cDNA encoding the ribulose-1,5-bisphosphate carboxylase/oxygenase from sunflower (Helianthus annuus). Nucleic Acids Res. 1987 Feb 11;15(3):1328–1328. doi: 10.1093/nar/15.3.1328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilson D. R., Larkins B. A. Zein gene organization in maize and related grasses. J Mol Evol. 1984;20(3-4):330–340. doi: 10.1007/BF02104739. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES