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. 1993 Dec;103(4):1291–1297. doi: 10.1104/pp.103.4.1291

DNA Replication-Dependent Histone H2A mRNA Expression in Pea Root Tips.

E Y Tanimoto 1, T L Rost 1, L Comai 1
PMCID: PMC159118  PMID: 12232021

Abstract

Histone H2A mRNA is selectively expressed in scattered subpopulations of cells in the pea (Pisum sativum) root apical meristem. To study whether this specific expression was associated with the cell cycle, a double-labeling technique was used to identify cells replicating DNA during S phase and those expressing H2A mRNA. Cells in S phase were detected by [3H]thymidine incorporation and autoradiography, whereas cells containing H2A mRNA were identified by in situ hybridization using digoxigenin-labeled probes. Approximately 92% of the [3H]thymidine-labeled S-phase cells expressed H2A mRNA and 85% of cells that expressed H2A mRNA were in S phase. In root tissue located basal to the promeristem, synchronous co-located expression was observed in scattered packets of proliferating cells. Furthermore, neither H2A mRNA nor S-phase cells could be detected within the quiescent center or mature root cap. When DNA synthesis was inhibited with hydroxyurea, a commensurate and specific decrease in steady-state levels of H2A mRNA was found. We conclude that cell-specific expression of pea histone H2A mRNA is replication dependent and that H2A mRNA is transiently accumulated during a period of the cell cycle that mostly overlaps the S phase. We propose that the overlap between H2A expression and S phase could occur if H2A mRNA accumulation began in late G1 and abated in late S.

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Selected References

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  1. Baumbach L. L., Stein G. S., Stein J. L. Regulation of human histone gene expression: transcriptional and posttranscriptional control in the coupling of histone messenger RNA stability with DNA replication. Biochemistry. 1987 Sep 22;26(19):6178–6187. doi: 10.1021/bi00393a034. [DOI] [PubMed] [Google Scholar]
  2. Butler W. B., Mueller G. C. Control of histone synthesis in HeLa cells. Biochim Biophys Acta. 1973 Feb 4;294(1):481–496. doi: 10.1016/0005-2787(73)90104-4. [DOI] [PubMed] [Google Scholar]
  3. Collart D., Ramsey-Ewing A., Bortell R., Lian J., Stein J., Stein G. Isolation and characterization of a cDNA from a human histone H2B gene which is reciprocally expressed in relation to replication-dependent H2B histone genes during HL60 cell differentiation. Biochemistry. 1991 Feb 12;30(6):1610–1617. doi: 10.1021/bi00220a024. [DOI] [PubMed] [Google Scholar]
  4. Harris M. E., Böhni R., Schneiderman M. H., Ramamurthy L., Schümperli D., Marzluff W. F. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol. 1991 May;11(5):2416–2424. doi: 10.1128/mcb.11.5.2416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hayashi S., Gillam I. C., Delaney A. D., Tener G. M. Acetylation of chromosome squashes of Drosophila melanogaster decreases the background in autoradiographs from hybridization with [125I]-labeled RNA. J Histochem Cytochem. 1978 Aug;26(8):677–679. doi: 10.1177/26.8.99471. [DOI] [PubMed] [Google Scholar]
  6. Hereford L. M., Osley M. A., Ludwig T. R., 2nd, McLaughlin C. S. Cell-cycle regulation of yeast histone mRNA. Cell. 1981 May;24(2):367–375. doi: 10.1016/0092-8674(81)90326-3. [DOI] [PubMed] [Google Scholar]
  7. Hereford L., Bromley S., Osley M. A. Periodic transcription of yeast histone genes. Cell. 1982 Aug;30(1):305–310. doi: 10.1016/0092-8674(82)90036-8. [DOI] [PubMed] [Google Scholar]
  8. Huh N. E., Hwang I. W., Lim K., You K. H., Chae C. B. Presence of a bi-directional S phase-specific transcription regulatory element in the promoter shared by testis-specific TH2A and TH2B histone genes. Nucleic Acids Res. 1991 Jan 11;19(1):93–98. doi: 10.1093/nar/19.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Krakoff I. H., Brown N. C., Reichard P. Inhibition of ribonucleoside diphosphate reductase by hydroxyurea. Cancer Res. 1968 Aug;28(8):1559–1565. [PubMed] [Google Scholar]
  10. Lycan D. E., Osley M. A., Hereford L. M. Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Feb;7(2):614–621. doi: 10.1128/mcb.7.2.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Martineau B., McBride K. E., Houck C. M. Regulation of metallocarboxypeptidase inhibitor gene expression in tomato. Mol Gen Genet. 1991 Aug;228(1-2):281–286. doi: 10.1007/BF00282477. [DOI] [PubMed] [Google Scholar]
  12. Marzluff W. F., Pandey N. B. Multiple regulatory steps control histone mRNA concentrations. Trends Biochem Sci. 1988 Feb;13(2):49–52. doi: 10.1016/0968-0004(88)90027-8. [DOI] [PubMed] [Google Scholar]
  13. Morris T. D., Weber L. A., Hickey E., Stein G. S., Stein J. L. Changes in the stability of a human H3 histone mRNA during the HeLa cell cycle. Mol Cell Biol. 1991 Jan;11(1):544–553. doi: 10.1128/mcb.11.1.544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Paddock S., Mahoney S., Minshall M., Smith L., Duvic M., Lewis D. Improved detection of in situ hybridization by laser scanning confocal microscopy. Biotechniques. 1991 Oct;11(4):486–493. [PubMed] [Google Scholar]
  16. Pokalsky A. R., Hiatt W. R., Ridge N., Rasmussen R., Houck C. M., Shewmaker C. K. Structure and expression of elongation factor 1 alpha in tomato. Nucleic Acids Res. 1989 Jun 26;17(12):4661–4673. doi: 10.1093/nar/17.12.4661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Russev G., Hancock R. Assembly of new histones into nucleosomes and their distribution in replicating chromatin. Proc Natl Acad Sci U S A. 1982 May;79(10):3143–3147. doi: 10.1073/pnas.79.10.3143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Stillman B. Chromatin assembly during SV40 DNA replication in vitro. Cell. 1986 May 23;45(4):555–565. doi: 10.1016/0092-8674(86)90287-4. [DOI] [PubMed] [Google Scholar]
  19. Tanimoto E., Douglas C., Halperin W. Factors Affecting Crown Gall Tumorigenesis in Tuber Slices of Jerusalem Artichoke (Helianthus tuberosus, L.). Plant Physiol. 1979 Jun;63(6):989–994. doi: 10.1104/pp.63.6.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Terada R., Nakayama T., Iwabuchi M., Shimamoto K. A wheat histone H3 promoter confers cell division-dependent and -independent expression of the gus A gene in transgenic rice plants. Plant J. 1993 Feb;3(2):241–252. doi: 10.1046/j.1365-313x.1993.t01-16-00999.x. [DOI] [PubMed] [Google Scholar]
  21. Van't Hof J. Cell population kinetics of excised roots of Pisum sativum. J Cell Biol. 1965 Oct;27(1):179–189. doi: 10.1083/jcb.27.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Worcel A., Han S., Wong M. L. Assembly of newly replicated chromatin. Cell. 1978 Nov;15(3):969–977. doi: 10.1016/0092-8674(78)90280-5. [DOI] [PubMed] [Google Scholar]

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