Abstract
Formation of the generative cell in flowering plants initiates the male spermatogenesis pathway which eventually culminates in the process of double fertilization. Little is known about the molecular mechanisms operative in the generative cell. Here, we report the isolation and characterization of cDNA clones encoding generative cell-specific histones, gcH2A and gcH3. In situ hybridization analysis revealed that both genes are activated after formation of the generative cell and accumulation of transcripts increases progressively during generative cell maturation. These results suggest that gcH2A and gcH3 mRNAs are products of transcriptional activation of the generative cell nucleus and thus provide the first evidence for male germ line cell-specific gene expression in flowering plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Blomstedt CK, Knox RB, Singh MB: Generative cells of Lilium longiflorum possess translatable mRNA and functional protein synthesis machinery. Plant Mol Biol 31: 1083–1086 (1996).
Bouget F, Gerttula S, Kloareg B, Quatrano R: A new nonradioactive in situ hybridization protocol for Fucus (Phaeophyta) embryos. J Phycol 31: 1027–1030(1995).
Bouget F, Gerttula S, Shaw SL, Quatrano R: Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryo. Plant Cell 8: 189–201(1996).
Chaibet N, Chaboute ME, Philipps G, Gigot C: Histone genes in higher plants: organisation and expression. Dev Genet. 8: 461–473(1987).
Choi YC, Gu W, Hecht NB, Feinberg AP, Chae CB: Molecular cloning of mouse somatic and testis-specific H2B histone genes containing a methylated CpG island. DNA Cell Biol 15: 495–504(1996).
Choi YC, Chae CB: DNA hypomethylation and germ cellspecific expression of testis-specific H2B histone gene. J Biol Chem 266: 20504–20511(1991).
Doenecke D, Albig W, Bode C, Drabent B, Franke K, Gavenis K, Witt O: Histones: genetic diversity and tissue-specific gene expression. Histochem. Cell Biol 107: 1–10(1997).
Doenecke D, Drabent B: Histone gene expression during mammalian spermatogenesis: structural and functional aspects. Mem Mus Natn Hist Nat 166, 525–535(1995).
Huh HG, Nakayama T, Meshi T, Iwabuchi M: Structural characteristics of two wheat histone H2A genes encoding distinct types of variants and functional differences in their promoter activity. Plant Mol Biol 33: 791–802(1997).
Koning AJ, Tanimoto EY, Kiehne K, Rost T, Comai L: Cellspecific expression of plant histone H2A genes. Plant Cell 3: 657–665(1991).
La Cour LF: Nuclear differentiation in the pollen grains. Heredity 3: 319–337(1949).
Lim K, Chae CB: Presence of a repressor protein for testisspecific H2B (TH2B) histone gene in early stages of spermatogenesis. J Biol Chem 267: 15271–15273(1992).
Mascarenhas JP: The biochemistry of angiosperm pollen development. Bot Rev 41: 259–314(1975).
McCormick S: Male gametephyte development. Plant Cell 5: 1265–1275(1993).
Oakeley EJ, Jost J-P: Non-symmetrical cytosine methylation in tobacco pollen. Plant Mol Biol 31: 927–930(1994).
Oakeley EJ, Podesta A, Jost J-P: Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc Natl Acad Sci USA 94: 11721–11725 (1997).
Osley MA: The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60: 827–851(1991).
Philpott A, Leno GH, Laskey RA: Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 65: 569–578(1991).
Philpott A, Leno GH: Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69: 759–767(1992).
Poccia DL: Remodelling of nucleoproteins during gametogenesis, fertilization and early development. Int Rev Cytol 105: 1–65(1986).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467(1977).
SheridanWF: Non-aqueous isolation of nuclei from lily pollen and examination of their histones. Z Pflanzenphysiol 450–459 (1972).
Spiker S, Weiβhaar B, da Costa e Silva O, Hahlbrock, K: Sequence of a histone H2A cDNA from parsley. Nucl Acids Res 18: 897 (1990).
Suzuki M: The DNA-binding motif, SPKK, and its variants. Nucl Acids Mol Biol 5: 126–140(1991).
Tanaka I: Isolation of generative cells and their protoplasts from pollen of Lilium longiflorum.Protoplasma 142: 68–73 (1988).
Tanaka I: Differentiation of generative and vegetative cells in angiosperm pollen. Sex Plant Reprod 10: 1–7(1997).
Terasaka O, Niitsu T: Unequal cell division and chromatin differentiation in pollen grain cells. Bot Mag Tokyo 102: 143–147(1987).
Torres MA, Rigai J, Puigdomenech P, Stiefel V: Specific distribution of mRNAs in maize growing pollen tubes observed by whole-mount in situ hybridization with non-radioactive probes. Plant J 8: 317–321(1995).
Thiebaid CH, Ruch F: Cytophotometric study of nuclear differentiation during pollen development in Tradescantia paludosa.Histochemistry 57: 119–128(1978).
Thomas G, Padayatty JD: Organization and bidirectional transcription of H2A, H2B and H4 histone genes in rice embryos. Nature, 306: 82–84(1983).
Ueda K, Miyamoto Y, Tanaka I: Fusion studies of pollen protoplasts and generative cell protoplasts in Lilium longiflorum. Plant Sci 72: 259–266(1990).
Ueda K, Tanaka I: The basic proteins of male gametic nuclei isolated from pollen grains of Lilium longiflorum.Planta 192: 446–452(1994).
Ueda K, Tanaka I: Male gametic nucleus-specific H2B and H3 histones, designated gH2B and gH3, in Lilium longiflorum. Planta 197: 289–295(1995).
Ueda K, Tanaka I: The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. Dev Biol 169: 210–217(1995).
Wu SC, Bogre L, Vincze E, Kiss GB, Dudits D: Isolation of alfalfa histone H3 gene: structure and expression. Plant Mol Biol 11: 641–649(1988).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Xu, H., Swoboda, I., Bhalla, P.L. et al. Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol Biol 39, 607–614 (1999). https://doi.org/10.1023/A:1006162120037
Issue Date:
DOI: https://doi.org/10.1023/A:1006162120037