Skip to main content
Log in

Unique positioning of mitochondria in developing microspores and pollen grains inPharbitis nil: mitochondria cover the nuclear surface at specific developmental stages

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Changes in the number and distribution of mitochondria in microspores and pollen grains during male gametogenesis inPharbitis nil were examined with Technovit sections stained with 3,3′-dihexyloxacarbocyanine iodide. The number of mitochondria per microspore or pollen grain ofP. nil increased constantly and dramatically during male gametogenesis. During this process, mitochondria exhibited characteristic localizations: subpopulations of mitochondria covered the surface of the microspore and vegetative nuclei before and again just after postmeiotic mitosis I (9 and 5 days before flowering, respectively). The mitochondria also surrounded the generative nucleus 2 days after postmeiotic mitosis I (5 days before flowering), although the density of mitochondria on the nuclear surface was lower. Electron microscopy showed that the mitochondria were about 30 nm from the nuclear envelope and that each mitochondrion was located near a nuclear pore. The characteristic localization of mitochondria inP. nil pollen may serve as a model to analyze the mechanisms that control mitochondrial positioning within a cell and interactions between mitochondria and nuclei.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

DAPI:

4′,6-diamidino-2-phenylindole

DiOC6 :

3,3′-dihexyloxacarbocyanine iodide

PM I:

postmeiotic mitosis I

References

  • Bednara J, Gielwanowska I, Rodkiewicz B (1986) Regular arrangements of mitochondria and plastids during sporogenesis inEquisetum. Protoplasma 130: 145–152

    Google Scholar 

  • Dickinson HG (1981) The structure and chemistry of plastid differentiation during male meiosis inLillian henryi. J Cell Sci 52: 223–241

    Google Scholar 

  • —, Li FL (1988) Organelle behaviour during higher plant gametogenesis. In: Boffey SA, Lloyd D (eds) The division and segregation of organelles. Cambridge University Press. Cambridge, pp 131–148

    Google Scholar 

  • —, Potter U (1979) Post-meiotic nucleo-cytoplasmic interaction inCosmos bipinnatus. Planta 145: 449–457

    Google Scholar 

  • Hagemann R, Schröder MB (1989) The cytological basis of the plastid inheritance in angiosperms. Protoplasma 152: 57–64

    Google Scholar 

  • Hu S, Zhu C, Xu L, Shen J (1979) Ultrastructure of male gametophyte in wheat I: the formation of generative and vegetative cells. Acta Bot Sin 21: 208–214

    Google Scholar 

  • Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999a) Decrease in mitochondrial DNA and concurrent increase in plastid DNA in generative cells ofPharbitis nil during pollen development. Eur J Cell Biol 78: 241–248

    Google Scholar 

  • — — — — — (1999b) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209: 53–65

    Google Scholar 

  • Owens JN, Morris SJ (1990) Cytological basis for cytoplasmic inheritance inPseudotsuga menziesii I: pollen tube and archegonial development. Am J Bot 77: 433–445

    Google Scholar 

  • Pacini E, Taylor PE, Singh MB, Knox RB (1992) Development of plastids in pollen and tapetum of rye-grass,Lolium perenne L. Ann Bot 70: 179–188

    Google Scholar 

  • Reynolds TL, Raghavan V (1982) An autoradiographic study of RNA synthesis during maturation and germination of pollen grains ofHyoscyamus niger. Protoplasma 111: 177–188

    Google Scholar 

  • Rodkiewicz B, Bednara J, Mostowska A, Duda E, Stobiecka H (1986) The change in disposition of plastids and mitochondria during microsporogenesis and sporogenesis in some higher plants. Acta Bot Neerl 35: 209–215

    Google Scholar 

  • Russell SD, Strout GW, Stramski AK, Mislan TW, Thompson RA, Schoemann LM (1996) Microgametogenesis inPlumbago zeylanica (Plumbaginaceae) 1: descriptive cytology and three-dimensional organization. Am J Bot 83: 1435–1453

    Google Scholar 

  • Saito C, Fujie M, Sakai A, Nagata N, Matsunaga S, Kuroiwa H, Kuroiwa T (1998) A high density of rRNA in the generative cells and sperm cells of pollen grains of five angiosperm species. Cytologia 63: 293–300

    Google Scholar 

  • Schröder MB, Oldenburg H (1990) Ultrastructural studies on plastids of generative and vegetative cells inLiliaceae 7: plastid distribution during generative cell development inTulbaghia violacea Harv. Flora 184: 131–136

    Google Scholar 

  • Sodmergen, Luo YY, Kuroiwa T, Hu SY (1994) Cytoplasmic DNA apportionment and plastid differentiation during male gametophyte development inPelargonium zonale. Sex Plant Reprod 7: 51–56

    Google Scholar 

  • —, Chen GH, Hu ZM, Guo FL, Guan XL (1995) Male gametophyte development inPlumbago zeylanica: cytoplasm localization and cell determination in the early generative cell. Protoplasma 186: 79–86

    Google Scholar 

  • Tanaka I (1991) Microtuble-determined plastid distribution during microsporogenesis inLilium longiflorum. J Cell Sci 99: 21–31

    Google Scholar 

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

    Google Scholar 

  • Terasaki M, Song J, Wong JR, Weiss MJ, Chen LB (1984) Localization of endoplasmic reticulum in living and glutaraldehyde-fixed cells with fluorescent dyes. Cell 38: 101–108

    Google Scholar 

  • Wagner VT, Cresti M, Salvatici P, Tiezzi A (1990) Changes in volume, surface area, and frequency of nuclear pores on the vegetative nucleus of tobacco pollen in fresh, hydrated, and activated conditions. Planta 181: 304–309

    Google Scholar 

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

    Google Scholar 

  • — — — — (1999b) Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol Biol 39: 607–614

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Nagata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nagata, N., Saito, C., Sakai, A. et al. Unique positioning of mitochondria in developing microspores and pollen grains inPharbitis nil: mitochondria cover the nuclear surface at specific developmental stages. Protoplasma 213, 74–82 (2000). https://doi.org/10.1007/BF01280507

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01280507

Keywords

Navigation