Skip to main content
SpringerLink
Log in

Generative cell–specific activation of the histone gH2A gene promoter of Lilium longiflorum in tobacco

  • Original Article
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

The Lilium longiflorum gH2A promoter is active exclusively in the generative cells of mature pollen in transgenic tobacco expressing the gH2A promoter::GUS (β-glucuronidase) construct as a reporter gene. Temporal and spatial aspects of gH2A promoter activity examined during pollen development in transgenic tobacco reveal that GUS reporter activity was not detected until developing pollen entered the early bicellular developmental stage. Activity was first detected in generative cells at early-mid stages and gradually increased to maximum levels at mid-bicellular stages. The patterns of appearance and longevity of GUS activity in tobacco were very similar to those of gH2A mRNA during pollen development in Lilium. Exogenous treatment with colchicine, a well-known microtubule depolymerize, blocked microspore mitosis and inhibited generative cell differentiation. No GUS signal was detected in the resulting anomalous pollen, which lacked generative cell differentiation. These data strongly suggest that normal generative cell development is essential for activation of the gH2A promoter. Furthermore, these results indicate that common transcriptional activator(s) of the gH2A promoter may be present in both Lilium and Nicotiana, and that such putative factor(s) activates the gH2A promoter only when generative cells undergo normal development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Berger F, Hamamura Y, Ingouff M, Higashiyama T (2008) Double fertilization—caught in the act. Trends Plant Sci 13:437–443

    Article  PubMed  CAS  Google Scholar 

  • Biedenkapp H, Borgmeyer U, Sippel AE, Klempnauer K-H (1988) Viral myb oncogene encodes a sequence-specific DNA binding activity. Nature 335:835–837

    Article  PubMed  CAS  Google Scholar 

  • Boavida LC, Becker JD, Feijó JA (2005) The making of gametes in higher plants. Int J Dev Biol 49:595–614

    Article  PubMed  CAS  Google Scholar 

  • Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478

    Article  PubMed  CAS  Google Scholar 

  • Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23:534–549

    Article  PubMed  CAS  Google Scholar 

  • Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5:e1000430

    Article  PubMed  Google Scholar 

  • Chen YC, McCormick S (1996) Sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122:3243–3253

    PubMed  CAS  Google Scholar 

  • Chen Z, Hafidh S, Poh SH, Twell D, Berger F (2009) Proliferation and cell fate establishment during Arabidopsis male gametogenesis depends on the Retinoblastoma protein. Proc Natl Acad Sci USA 106:7257–7262

    Article  PubMed  CAS  Google Scholar 

  • Dickinson HG, Grant-Downton R (2009) Bridging the generation gap: flowering plant gametophytes and animal germlines reveal unexpected similarities. Biol Rev Camb Philos Soc 84:589–615

    Article  PubMed  Google Scholar 

  • Eady C, Lindsey K, Twell D (1995) The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7:65–74

    PubMed  CAS  Google Scholar 

  • Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm: identification of male gamete promoters in Arabidopsis thaliana. Plant Physiol 138:2124–2133

    Article  PubMed  CAS  Google Scholar 

  • Haerizadeh F, Singh MB, Bhalla PL (2006) Transcriptional repression distinguishes somatic from germ cell lineages in a plant. Science 313:496–499

    Article  PubMed  CAS  Google Scholar 

  • Hafidh S, Breznenová1 K, Růžička P, Feciková J, Čapková V, Honys D (2012) Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol 12:24

    Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y, Cresti M, Tiezzi A, Moscatelli A (1988) Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube. J Cell Sci 91:49–60

    Google Scholar 

  • Honys D, Reňák D, Twell D (2006) Male gametophyte development and function. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, 1st edn. Global Science Books, London, pp 76–87

  • Kim HJ, Ok SH, Bahn SC, Jang J, Oh SA, Park SK, Twell D, Ryu SB, Shin JS (2011) Endoplasmic reticulum- and golgi-localized phospholipase A2 plays critical roles in Arabidopsis pollen development and germination. Plant Cell 23:94–110

    Article  PubMed  CAS  Google Scholar 

  • Kyo M, Hattori S, Yamaji N, Pechan P, Fukui H (2003) Cloning and characterization of cDNAs associated with the embryogenic dedifferentiation of tobacco immature pollen grains. Plant Sci 164:1057–1066

    Article  CAS  Google Scholar 

  • Matsushima R, Hamamura Y, Higashiyama T, Arimura S, Sodmergen T, Tsutsumi N, Sakamoto W (2008) Mitochondrial dynamics in plant male gametophyte visualized by fluorescent live imaging. Plant Cell Physiol 49:1074–1083

    Article  PubMed  CAS  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16:S142–S153

    Article  PubMed  CAS  Google Scholar 

  • Metzinger CA, Bergmann DC (2010) Plant asymmetric cell division regulators: pinch-hitting for PARs? F1000 Biol Rep 2:25

    Google Scholar 

  • Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2005) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71

    Article  PubMed  Google Scholar 

  • Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79:639–648

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Park KS, Twell D, Park SK (2010) The SIDECAR POLLEN gene encodes a microspore-specific LOB/AS2 domain protein required for the correct timing and orientation of asymmetric cell division. Plant J 64:839–850

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Twell D, Park SK (2011) SIDECAR POLLEN suggests a plant-specific regulatory network underlying asymmetric microspore division in Arabidopsis. Plant Signal Behav 6:416–419

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Bhalla PL, Singh MB (2005a) Transcriptional activity of male gamete-specific histone gcH3 promoter in sperm cells of Lilium longiflorum. Plant Cell Physiol 46:797–802

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Endo M, Singh MB, Bhalla PL (2005b) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44:557–568

    Article  PubMed  CAS  Google Scholar 

  • Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799

    PubMed  CAS  Google Scholar 

  • Reňák D, Dupl’áková N, Honys D (2011) Wide-scale screening of T-DNA lines for transcription factor genes affecting male gametophyte development in Arabidopsis. Sex Plant Reprod. doi:10.1007/s00497-011-0178-8

  • Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248

    Article  PubMed  CAS  Google Scholar 

  • Russell SD, Cass DD (1981) Ultrastructure of the sperms of Plumbago zeylanica. 1. Cytology and association with the vegetative nucleus. Protoplasma 107:85–107

    Article  Google Scholar 

  • Scheres B, Benfey PN (1999) Asymmetric cell division in plants. Annu Rev Plant Physiol Plant Mol Biol 50:505–537

    Article  PubMed  CAS  Google Scholar 

  • Singh M, Bhalla PL, Xu H, Singh MB (2003) Isolation and characterization of a flowering plant male gametic cell-specific promoter. FEBS Lett 542:47–52

    Article  PubMed  CAS  Google Scholar 

  • Singh MB, Bhalla PL, Russell SD (2008) Molecular repertoire of flowering plant male germ cells. Sex Plant Reprod 20:27–36

    Article  Google Scholar 

  • Tanaka I (1997) Differentiation of generative and vegetative cells in angiosperm pollen. Sex Plant Reprod 10:1–7

    Article  Google Scholar 

  • Tanaka I, Nakamura S, Miki-Hirosige H (1989) Structural features of isolated generative cells and their protoplasts from pollen of some liliaceous plants. Gamete Res 24:361–374

    Article  PubMed  CAS  Google Scholar 

  • Tanaka I, Ono K, Fukuda T (1998) The developmental fate of angiosperm pollen is associated with a preferential decrease in the level of histone H1 in the vegetative nucleus. Planta 206:561–569

    Article  CAS  Google Scholar 

  • Tebbutt SJ, Rogers HJ, Lonsdale DM (1994) Characterization of a tobacco gene encoding a pollen-specific polygalacturonase. Plant Mol Biol 25:283–297

    Article  PubMed  CAS  Google Scholar 

  • Twell D (1994) The diversity and regulation of gene expression in the pathway of male gametophyte development. In: Scott RJ, Stead AD (eds) Molecular and cellular aspects of plant reproduction. Seminar series 55, Cambridge University Press, Cambridge, pp 83–135

  • Twell D (2010) Male gametophyte development. In: Pua EC, Davey MR (eds) Plant developmental biology-biotechnological perspectives vol 1. Springer-Verlag Berlin, pp 225–244

  • Twell D (2011) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24:149–160

    Article  PubMed  Google Scholar 

  • Twell D, Patel S, Sorensen A, Roberts M, Scott R, Draper J, Foster G (1993) Activation and developmental regulation of on Arabidopsis anther-specific promoter in microspores and pollen of Nicotiana tabacum. Sex Plant Reprod 6:217–224

    Article  Google Scholar 

  • Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  • Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4:711–714

    Article  PubMed  CAS  Google Scholar 

  • Ueda K, Tanaka I (1995) The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. Dev Biol 169:210–217

    Article  PubMed  CAS  Google Scholar 

  • Ueda K, Kinoshita Y, Xu ZJ, Ide N, Ono M, Akahori Y, Tanaka I, Inoue M (2000) Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum. Chromosoma 108:491–500

    Article  PubMed  CAS  Google Scholar 

  • Ueda K, Suzuki M, Ono M, Ide N, Tanaka I, Inoue M (2005) Male gametic cell-specific histone gH2A gene of Lilium longiflorum: genomic structure and promoter activity in the generative cell. Plant Mol Biol 59:229–238

    Article  PubMed  CAS  Google Scholar 

  • Xin HP, Peng XB, Ning J, Yan TT, Ma LG, Sun MX (2011) Expressed sequence-tag analysis of tobacco sperm cells reveals a unique transcriptional profile and selective persistence of paternal transcripts after fertilization. Sex Plant Reprod 24:37–46

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Swoboda I, Bhalla PL, Singh MB (1999) Male gametic cell-specific gene expression in flowering plants. Proc Natl Acad Sci USA 96:2554–2558

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Weterings K, Vriezen W, Feron R, Xue Y, Derksen J, Mariani C (2002) Isolation and characterization of male-germ-cell transcripts in Nicotiana tabacum. Sex Plant Reprod 14:339–346

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank K. Toyosawa for excellent technical assistance.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Faculty of Bioresource Sciences, Akita Prefectural University, Akita, 010-0195, Japan

    Kenji Ueda, Jun Iwashita, Hiroetsu Wabiko & Masayasu Inoue

  2. Gene Research Center, University of Tsukuba, Ibaraki, 305-8572, Japan

    Michiyuki Ono

Authors
  1. Kenji Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michiyuki Ono
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Iwashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroetsu Wabiko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masayasu Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenji Ueda.

Additional information

Communicated by David Twell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ueda, K., Ono, M., Iwashita, J. et al. Generative cell–specific activation of the histone gH2A gene promoter of Lilium longiflorum in tobacco. Sex Plant Reprod 25, 247–255 (2012). https://doi.org/10.1007/s00497-012-0194-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-012-0194-3

Keywords

Search

Navigation