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. 1995 Sep 25;23(18):3756–3763. doi: 10.1093/nar/23.18.3756

The uni chromosome of Chlamydomonas: histone genes and nucleosome structure.

Z Walther 1, J L Hall 1
PMCID: PMC307276  PMID: 7479007

Abstract

The uni linkage group (ULG) of Chlamydomonas reinhardtii contains many genes involved in the basal body-flagellar system. Recent evidence suggests that the corresponding uni chromosome is located in close proximity to the basal body complex. In the course of studies into its molecular organization, we have found a cluster of four histone genes on the ULG. The genes are arranged as divergently-transcribed pairs: H3-H4 and H2B-H2A. Genomic sequencing reveals that these genes lack introns and contain characteristic 3' palindromes similar to those of animals. The predicted amino acid sequences are highly conserved across species, with greatest similarities to the histone genes of Volvox. Southern analysis shows that each histone gene is present in 15-20 copies in Chlamydomonas and suggests a dispersed genomic organization. Northern analysis of mitotically-synchronized cells shows that, like the replication-dependent histones of higher eukaryotes, Chlamydomonas histone genes are expressed during S-phase. Using a gene-specific probe on Northern blots, we provide evidence that the ULG H4 gene is regulated in the same manner as other Chlamydomonas histone genes. Finally, micrococcal nuclease protection experiments show that the uni chromosome itself associates with histone proteins and displays a conventional nucleosomal banding pattern.

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Selected References

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

  1. Ares M., Jr, Howell S. H. Cell cycle stage-specific accumulation of mRNAs encoding tubulin and other polypeptides in Chlamydomonas. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5577–5581. doi: 10.1073/pnas.79.18.5577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cavalier-Smith T. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci. 1974 Dec;16(3):529–556. doi: 10.1242/jcs.16.3.529. [DOI] [PubMed] [Google Scholar]
  3. Debuchy R., Purton S., Rochaix J. D. The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J. 1989 Oct;8(10):2803–2809. doi: 10.1002/j.1460-2075.1989.tb08426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dutcher S. K., Galloway R. E., Barclay W. R., Poortinga G. Tryptophan analog resistance mutations in Chlamydomonas reinhardtii. Genetics. 1992 Jul;131(3):593–607. doi: 10.1093/genetics/131.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dutcher S. K., Power J., Galloway R. E., Porter M. E. Reappraisal of the genetic map of Chlamydomonas reinhardtii. J Hered. 1991 Jul-Aug;82(4):295–301. doi: 10.1093/oxfordjournals.jhered.a111089. [DOI] [PubMed] [Google Scholar]
  6. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  7. Hall J. L., Luck D. J. Basal body-associated DNA: in situ studies in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1995 May 23;92(11):5129–5133. doi: 10.1073/pnas.92.11.5129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hall J. L., Ramanis Z., Luck D. J. Basal body/centriolar DNA: molecular genetic studies in Chlamydomonas. Cell. 1989 Oct 6;59(1):121–132. doi: 10.1016/0092-8674(89)90875-1. [DOI] [PubMed] [Google Scholar]
  9. Harvey R. P., Robins A. J., Wells J. R. Independently evolving chicken histone H2B genes: identification of a ubiquitous H2B-specific 5' element. Nucleic Acids Res. 1982 Dec 11;10(23):7851–7863. doi: 10.1093/nar/10.23.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heintz N., Zernik M., Roeder R. G. The structure of the human histone genes: clustered but not tandemly repeated. Cell. 1981 Jun;24(3):661–668. doi: 10.1016/0092-8674(81)90092-1. [DOI] [PubMed] [Google Scholar]
  11. Johnson K. A., Rosenbaum J. L. Basal bodies and DNA. Trends Cell Biol. 1991 Dec;1(6):145–149. doi: 10.1016/0962-8924(91)90002-q. [DOI] [PubMed] [Google Scholar]
  12. Keller L. R., Schloss J. A., Silflow C. D., Rosenbaum J. L. Transcription of alpha- and beta-tubulin genes in vitro in isolated Chlamydomonas reinhardi nuclei. J Cell Biol. 1984 Mar;98(3):1138–1143. doi: 10.1083/jcb.98.3.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Maxson R., Cohn R., Kedes L., Mohun T. Expression and organization of histone genes. Annu Rev Genet. 1983;17:239–277. doi: 10.1146/annurev.ge.17.120183.001323. [DOI] [PubMed] [Google Scholar]
  14. Morris R. L., Keller L. R., Zweidler A., Rizzo P. J. Analysis of Chlamydomonas reinhardtii histones and chromatin. J Protozool. 1990 Mar-Apr;37(2):117–123. doi: 10.1111/j.1550-7408.1990.tb05880.x. [DOI] [PubMed] [Google Scholar]
  15. Müller K., Lindauer A., Brüderlein M., Schmitt R. Organization and transcription of Volvox histone-encoding genes: similarities between algal and animal genes. Gene. 1990 Sep 14;93(2):167–175. doi: 10.1016/0378-1119(90)90221-c. [DOI] [PubMed] [Google Scholar]
  16. Müller K., Schmitt R. Histone genes of Volvox carteri: DNA sequence and organization of two H3-H4 gene loci. Nucleic Acids Res. 1988 May 11;16(9):4121–4136. doi: 10.1093/nar/16.9.4121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Osley M. A., Gould J., Kim S., Kane M. Y., Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell. 1986 May 23;45(4):537–544. doi: 10.1016/0092-8674(86)90285-0. [DOI] [PubMed] [Google Scholar]
  18. Osley M. A. The regulation of histone synthesis in the cell cycle. Annu Rev Biochem. 1991;60:827–861. doi: 10.1146/annurev.bi.60.070191.004143. [DOI] [PubMed] [Google Scholar]
  19. Ramanis Z., Luck D. J. Loci affecting flagellar assembly and function map to an unusual linkage group in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1986 Jan;83(2):423–426. doi: 10.1073/pnas.83.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schloss J. A., Croom H. B. Normal Chlamydomonas nuclear gene structure on linkage group XIX. J Cell Sci. 1991 Dec;100(Pt 4):877–881. doi: 10.1242/jcs.100.4.877. [DOI] [PubMed] [Google Scholar]
  21. Schümperli D. Multilevel regulation of replication-dependent histone genes. Trends Genet. 1988 Jul;4(7):187–191. doi: 10.1016/0168-9525(88)90074-1. [DOI] [PubMed] [Google Scholar]
  22. Silflow C. D., Chisholm R. L., Conner T. W., Ranum L. P. The two alpha-tubulin genes of Chlamydomonas reinhardi code for slightly different proteins. Mol Cell Biol. 1985 Sep;5(9):2389–2398. doi: 10.1128/mcb.5.9.2389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sive H. L., Heintz N., Roeder R. G. Multiple sequence elements are required for maximal in vitro transcription of a human histone H2B gene. Mol Cell Biol. 1986 Oct;6(10):3329–3340. doi: 10.1128/mcb.6.10.3329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Walther Z., Vashishtha M., Hall J. L. The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J Cell Biol. 1994 Jul;126(1):175–188. doi: 10.1083/jcb.126.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wells D. E. Compilation analysis of histones and histone genes. Nucleic Acids Res. 1986;14 (Suppl):r119–r149. doi: 10.1093/nar/14.suppl.r119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Youngblom J., Schloss J. A., Silflow C. D. The two beta-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Mol Cell Biol. 1984 Dec;4(12):2686–2696. doi: 10.1128/mcb.4.12.2686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. de Hostos E. L., Schilling J., Grossman A. R. Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. Mol Gen Genet. 1989 Aug;218(2):229–239. doi: 10.1007/BF00331273. [DOI] [PubMed] [Google Scholar]

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