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Isolation and molecular characterization of gibberellin-regulated H1 and H2B histone cDNAs in the leaf of the gibberellin-deficient tomato

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Abstract

After differential screening we isolated cDNA clones encoding a histone H1 (leH1) and three variants of histone H2B (leH2B-1, -2 and -3) from the gibberellin (GA)-deficient mutant of tomato (gib-1). The deduced polypeptide of leH1 is 271 amino acids long and exhibits the typical tripartite structure of histones H1. The full-length cDNA clone leH2B-1 encodes for a protein of 142 amino residues and shows the tripartite organization of histones H2B. The histones leH1 and leH2B, which show no tissue specificity, are developmentally expressed in the leaf. The mRNA accumulation was higher in organs which contain meristematic tissue and/or which have a high proportion of actively cycling cells. In the leaf of the gib-1 mutant we demonstrated GA-enhanced histone leH1 and leH2B expression which was not observed in the wild type. GAs of the early-13-hydroxylated pathway (GA1 and GA3) caused most enhanced transcription compared to GAs of the early-non-hydroxylation pathway (GA4 and GA9). Application of GA to the mutant increased histone expression that could correlate with enhanced DNA replication in leaf tissue. Increased chromosome replication may indicate that there is a higher rate of cell division and/or increase of endopolyploidy which both may be dependent on cell elongation induced by GAs.

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References

  1. Ausio J, Dong F, Van Holde KE: Use of selectively trypsinized nucleosome core particles to analyze the role of the histone tails in the stabilization of the nucleosome. J Mol Biol 206: 451–463 (1989).

    PubMed  Google Scholar 

  2. Bensen RJ, Zeevaart JAD: Comparison of ent-kaurene synthetase A and B activities in cell-free extracts from young tomato fruits of wild-type and gib-1, gib-2, and gib-3 tomato plants. J Plant Growth Regul 9: 237–242 (1990).

    Google Scholar 

  3. Cavallini A, Baroncelli S, Lercari B, Cionini G, Rocca M, Amato FD: Effect of light and gibberellic acid on chromosome endoreduplication in leaf epidermis of Triticum durum DesfC. Protoplasma 186: 57–62 (1995).

    Google Scholar 

  4. Chandra Sekhar KN, Sawhney VK: Regulation of leaf shape in the Solanifolia mutant of tomato (Lycopersicon esculentum) by plant growth substances. Ann Bot 67: 3–6 (1991).

    Google Scholar 

  5. Chien JC, Sussex IM: Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol 111: 1321–1328 (1996).

    PubMed  Google Scholar 

  6. Cosgrove DJ, Sovonick-Dunford SA: Mechanism of gibberellin-dependent stem elongation in peas. Plant Physiol 89: 184–191 (1989).

    PubMed  Google Scholar 

  7. Crane-Robinson C, Ptitsyn OB: Binding of the globular domain of linker histones H5/H1 to the nucleosome: a hypothesis. Prot Engng 2: 577–582 (1989).

    Google Scholar 

  8. Davies KM, Seelye JF, Irving DE, Borst WM, Hurst PL, King GA: Sugar regulation of harvest-related genes in Asparagus. Plant Physiol 111: 877–883 (1996).

    PubMed  Google Scholar 

  9. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).

    PubMed  Google Scholar 

  10. Feinberg AP, Vogelstein B: A technique for radiolabelling DNA fragments to high specific activity. Anal Biochem 137: 266–267 (1984).

    PubMed  Google Scholar 

  11. Gantt JS, Key JL: Molecular cloning of a pea H1 histone cDNA. Eur J Biochem 166: 119–125 (1987).

    PubMed  Google Scholar 

  12. Gantt JS, Lenvik TR: Arabidopsis thaliana H1 histones, analysis of two members of a small gene family. Eur J Biochem 202: 1029–1039 (1991).

    PubMed  Google Scholar 

  13. Graebe JE: Gibberellin biosynthesis and control. Annu Rev Plant Physiol 38: 419–465 (1987).

    Google Scholar 

  14. Hill CS, Thomas J O: Core histone-DNA interactions in urchin sperm chromatin. The amino terminal tail of H2B interacts with linker DNA. Eur J Biochem 187: 145–153 (1990).

    PubMed  Google Scholar 

  15. Hill CS, Rimmer JM, Green BN, Finch JT, Thomas JO: Histone-DNA interactions and their modulation by phosphorylation of-Ser-Pro-X-Lys/Arg-motifs. EMBO J 10: 19391948 (1991).

    Google Scholar 

  16. Jacobsen SE, Olszewski NE: Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant. Plant Physiol 97: 409–414 (1991).

    Google Scholar 

  17. Jayawardene N, Riggs CD: Molecular cloning, sequence analysis and differential expression of an intron-containing gene encoding tomato histone H1. Eur J Biochem 223: 693–699 (1994).

    PubMed  Google Scholar 

  18. Joanin P, Gigot C, Philipps G: Nucleotide sequence and expression of two cDNA coding for two histone H2B variants of maize. Plant Mol Biol 20: 581–588 (1992).

    PubMed  Google Scholar 

  19. Joanin P, Gigot C, Philipps G: Molecular cloning and sequence analysis of two genes encoding two histone H2B variants of maize. Plant Physiol Biochem 32: 693–696 (1994).

    Google Scholar 

  20. Jupe SC, Causton DR, Scott IM: Cellular basis of the effects of gibberellin and the pro gene on stem growth in tomato. Planta 174: 106–111 (1988).

    Google Scholar 

  21. Kapros T, Stefanov I, Magyar Z, Ocsovsky I, Dudits D: A short histone H3 promoter from alfalfa species expression in S-phase cells and meristems. In Vitro Cell Devel Biol 29P: 27–32 (1993).

    Google Scholar 

  22. Kende H, Zeevaart JAD: The five 'classical' plant hormones. Plant Cell 9: 1197–1210 (1997).

    PubMed  Google Scholar 

  23. Khadake JR, Rao MRS: Preferential condensation of SARDNA by histone H1 and its SPKK containing octapeptide repeat motif. FEBS Lett 400: 193–196 (1997).

    PubMed  Google Scholar 

  24. Kobayashi M, Yamaguchi I, Murofushi N, Ota Y, Takahashi N: Fluctuation and localization of endogenous gibberellins in rice. Agric Biol Chem 52: 1189–1194 (1988).

    Google Scholar 

  25. Konings H, Berrevoets M, Nagel O, Lambers H: Growth rate and plant development of tomato gib mutants in relation to endogenous gibberellic acid. Acta Bot Neerl 41: 208 (1992).

    Google Scholar 

  26. Koornneef M, Bosma TDG, Hanhart CJ, Van der Veen JH, Zeevaart JAD: The isolation and characterization of gibberellin-deficient mutants in tomato. Theor Appl Genet 80: 852–857 (1990).

    Article  Google Scholar 

  27. Koshioka M, Nishijima T, Yamazaki H, Liu Y, Nonaka M, Mander LN: Analysis of gibberellins in growing fruits of Lycopersicon esculentum after pollination or treatment with 4-chlorophenoxyacetic acid. J Hort Sci 69: 171–179 (1994).

    Google Scholar 

  28. Liu PBW, Loy JB: Action of gibberellic acid on cell proliferation in the subapical shoot meristem of water melon seedlings. Am J Bot 63: 700–704 (1976).

    Google Scholar 

  29. Melaragno JE, Mehrotra B, Coleman AW: Relationship between endoploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668 (1993).

    Article  PubMed  Google Scholar 

  30. Metzger JD, Hassebrock AT: Selection and characterization of a gibberellin-deficient mutant of Thlaspi arvense L. Plant Physiol 94: 1655–1662 (1990).

    Google Scholar 

  31. Minami M, Huh GH, Yang P, Iwabuchi M: Coordinate gene expression of five subclass histones and the putative transcription factors, HBP-1a and HBP-1b, of histone genes in wheat. Plant Mol Biol 23: 429–434 (1993).

    PubMed  Google Scholar 

  32. Ohtsubo N, Nakayama T, Terada R, Shimamoto K, Iwabuchi M: Proximal promoter region of the wheat histone H3 gene confers S phase-specific gene expression in transformed rice cells. Plant Mol Biol 23: 553–565 (1993).

    PubMed  Google Scholar 

  33. Osley MA: The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60: 827–861 (1991).

    Article  PubMed  Google Scholar 

  34. Pharis RP, King RW: Gibberellins and reproductive development in seed plants. Annu Rev Plant Physiol 36: 517–568 (1985).

    Google Scholar 

  35. Phinney BO: Gibberellin A1, dwarfism and the control of shoot elongation in higher plants. In: Crozier A, Hillman J.R. (eds) The Biosynthesis and Metabolism of Plant Hormones. Society of Experimental Biology Seminar Series 23: 17–41. Cambridge University Press, Cambridge, UK (1984).

    Google Scholar 

  36. Poethig RC: Leaf Morphogenesis in flowering plants. Plant Cell 9: 1077–1087 (1997).

    PubMed  Google Scholar 

  37. Razafimahatratra P, Chaubet N, Philipps G, Gigot C: Nucleotide sequence and expression of a maize H1 histone cDNA. Nucl Acids Res 19: 1491–1496 (1991).

    PubMed  Google Scholar 

  38. Reeves II AF: Tomato trichomes and mutations affecting their development. Am J Bot 64: 186–189 (1977).

    Google Scholar 

  39. Reichheld J-P, Sonobe S, Clément B, Chaubet N, Gigot C: Cell cycle-regulated histone gene expression in synchronized plant cells. Plant J 7: 245–252 (1995).

    Article  Google Scholar 

  40. Reid JB: Internode length in Pisum: do the internode length genes effect growth in dark-grown plants? Plant Physiol 72: 759–763 (1983).

    Google Scholar 

  41. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  42. Sauter M, Kende H: Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188: 362–368 (1992).

    Google Scholar 

  43. Sheridan WF, Stern H: Histones of meiosis. Exp Cell Res 45: 323–335 (1967).

    PubMed  Google Scholar 

  44. Stuart DA, Durnam DJ, Jones RL: Cell elongation and cell division in elongating lettuce hypocotyl sections. Planta 135: 249–255 (1977).

    Google Scholar 

  45. Suzuki M: SPXX, a frequent sequence motif in gene regulatory proteins. J Mol Biol 207: 61–84 (1989).

    PubMed  Google Scholar 

  46. Szekeres M, Haizel T, Adam E, Nagy F: Molecular characterization and expression of a tobacco histone H1 cDNA. Plant Mol Biol 27: 597–605 (1995).

    PubMed  Google Scholar 

  47. Tanimoto EY, Rost TL, Comai L: DNA replication-dependent histone H2A mRNA expression in pea root tips. Plant Physiol 103: 1291–1297 (1993).

    PubMed  Google Scholar 

  48. Ueda K, Tanaka I: Male gametic nucleus-specific H2B and H3 histones, designated gH2B and gH3, in Lilium longiflorum. Planta 197: 289–295 (1995).

    Google Scholar 

  49. van Eldik GJ, Vriezen WH, Wingens M, Ruiter RK, van Herpen MMA, Schrauwen JAM, Wullems GJ: A pistil-specific gene of Solanum tuberosum is predominantly expressed in the stylar cortex. Sex Plant Reprod 8: 173–179 (1995).

    Google Scholar 

  50. Wells D, Brown D: Histone and histone gene compilation and alignment update. Nucl Acids Res 19: 2173–2188 (1991).

    PubMed  Google Scholar 

  51. Woo H-H, Brigham LA, Hawes MC: Molecular cloning and expression of mRNAs encoding H1 histone and H1 histonelike sequences in root tips of pea (Pisum sativum L.). Plant Mol Biol 28: 1143–1147 (1995).

    PubMed  Google Scholar 

  52. Waycott W, Taiz L: Phenotypic characterization of lettuce dwarf mutants and their response to applied gibberellins. Plant Physiol 95: 1162–1168 (1991).

    Google Scholar 

  53. Yang P, Katsura M, Nakayama T, Mikami K, Iwabuchi M: Molecular cloning and nucleotide sequences of cDNAs for histone H1 and H2B variants from wheat. Nucl Acids Res 19: 5077–5077 (1991).

    PubMed  Google Scholar 

  54. Yang P, Taoka K-I, Nakayama T, Iwabuchi M: Structural and functional characterization of two wheat histone H2B promoters. Plant Mol Biol 28: 155–172 (1995).

    PubMed  Google Scholar 

  55. Zanewich KP, Rood SB, Williams PH: Growth and development of Brassica genotypes differing in endogenous gibberellin content. I. Leaf reproductive development. Physiol Plant 79: 673–678 (1990).

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Experimental Botany, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, Netherlands

    K.J.P.T. van den Heuvel, R.J. van Esch, G.W.M. Barendse & G.J. Wullems

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  1. K.J.P.T. van den Heuvel
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  2. R.J. van Esch
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  3. G.W.M. Barendse
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  4. G.J. Wullems
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van den Heuvel, K., van Esch, R., Barendse, G. et al. Isolation and molecular characterization of gibberellin-regulated H1 and H2B histone cDNAs in the leaf of the gibberellin-deficient tomato. Plant Mol Biol 39, 883–890 (1999). https://doi.org/10.1023/A:1006157718263

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