Skip to main content
Log in

Histology of sterile male and female cones in Pinus monticola (western white pine)

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

Abstract

Two years of histological samples were collected from a Pinus monticola Dougl. (western white pine) tree identified as not producing mature pollen or seed cones. Anatomical information was collected to the ultrastructural level, to assess possible mechanisms for pollen and cone abortion resulting in sterility. Development of male and female gametophytes in the sterile western white pine tree was arrested after meiosis and before further cell divisions could take place. Sterile male gametophytes (pollen grains) had poorly developed pollen walls and sacci, reduced and degenerative cytoplasm, and no evidence of stored starch grains. The pollen cone aborted prior to pollen dehiscence. Meiosis of the megaspore mother cell in the ovule produced four megaspores, but development was stopped at the functional megaspore stage. The seed cone aborted in the first year of growth before winter dormancy. Tapetal tissue in sterile microsporangia appeared similar to that of fertile microsporangia, until the vacuolate, uninucleate microspore stage. Tapetal cells and thecal fluid surrounding the sterile microspores persisted well past the time when microsporangia on fertile trees started the process of maturation and desiccation. At pollen dehiscence, sterile pollen cones did not release any pollen and the microsporangia were filled with a sticky fluid. The behaviour of the tapetum in P. monticola sterile cones is compared with reports of tapetal function and malfunction reported in studies of angiosperm and other gymnosperm species. The occurrence and timing of gametophyte abortion in both cone sexes suggests a genetic rather than environmental basis for the sterility mechanism.

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.

Fig. 1a–f.
Fig. 2a–f.
Fig. 3a–f.
Fig. 4a, b.

Similar content being viewed by others

References

  • Anderson EA, Owens JN (2000) Microsporogenesis, pollination, pollen germination and male gametophyte development in Taxus brevifolia. Ann Bot 86:1033–1042

    Article  Google Scholar 

  • Andersson EA (1947) Case of asyndesis in Picea abies. Heredity 33:301–347

    Google Scholar 

  • Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, Iowa

  • Cecchi Fiordi A, Lippi MM, Tani G (1991) Ultrastructural observations on the megasporocyte of Taxus baccata L. (Taxaceae) in relation to megaspore behaviour. Caryologia 44:45–53

    Google Scholar 

  • Chapman GP (1987) The tapetum. Int Rev Cytol 107:111–125

    Google Scholar 

  • Chen Z-K, Wang F-X, Zhou F (1987) Investigation on the ultrastructure of the tapetum in Pinus bungeana. Acta Bot Sin 29:486–491

    Google Scholar 

  • Cigan AM, Unger E, Xui R-J, Kendall T, Fox TW (2001) Phenotypic complementation of ms45 maize requires tapetal expression of MS45. Sex Plant Reprod 14:135–142

    CAS  Google Scholar 

  • Corti EF, Maugini E (1964) Solid bodies passing from tapetum to central cell in Pinus pinea archegonium. Caryologia 17:1–39

    Google Scholar 

  • Eis S, Garman EH, Ebell LF (1965) Relation between cone production and diameter increment of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco), grand fir (Abies grandis (Dougl.) Lindl.), and western white pine (Pinus monticola Dougl.). Can J Bot 43:1553–1559

    Google Scholar 

  • El-Kassaby UA, Barclay HJ (1992) Cost of reproduction in Douglas-fir. Can J Bot 70:1429–1432

    Google Scholar 

  • Ellis MF, Sedgley M (1993) Gynodioecy and male sterility in Eucalyptus leucoxylon F. Muell. (Myrtaceae). Int J Plant Sci 154:314–324

    Article  Google Scholar 

  • Gifford EM (1950) Softening refractory plant material embedded in paraffin. Stain Technol 25:161–162

    Google Scholar 

  • Heslop-Harrison J (1971) The pollen wall: structure and development. In: Heslop-Harrison J (ed) Pollen development and physiology. Butterworths, London, pp 75–98

  • Ilarslan H, Horner HT, Palmer RG (1999) Genetics and cytology of a new male-sterile, female-fertile soybean mutant. Crop Sci 39:658–664

    Google Scholar 

  • Jin W, Horner HT, Palmer RG (1997) Genetics and cytology of a new genic male-sterile soybean (Glycine max (L.) Merr.). Sex Plant Reprod 10:13–21

    Article  Google Scholar 

  • Johansen DA (1940) Plant Microtechnique. McGraw-Hill, New York

  • Lalonde S, Beebe DU, Saini HS (1997) Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit. Sex Plant Reprod 10:40–48

    Article  Google Scholar 

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38:425–454

    Google Scholar 

  • Malik CP, Walia K (1981) Male sterility. Recent Adv Pollen Res 171–200

  • Mascarenhas JP (1990). Gene activity during pollen development. Annu Rev Plant Physiol Plant Mol Biol 41:317–338

    Article  Google Scholar 

  • Mouradov A, Teasdale RD (1999) Family of genes involved at the early stages of 'flower' development in radiata pine. Flowering Newslett 27:16–22

    Google Scholar 

  • Nishiyama I (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. VII. Electron microscopical observations on tapetal cells dilated by the cooling treatment. Proc Crop Sci Soc Japan 39:480–486

    Google Scholar 

  • Orr-Ewing AL (1977) Female sterility in Douglas fir. Silvae Genet 26:75–77

    Google Scholar 

  • Orr-Ewing AL (1978) Partial male sterility in Douglas fir. Province of British Columbia Ministry of Forests Research Memo 35

  • Owens JN, Bruns D (2000) Western white pine (Pinus monticola Dougl.) reproduction. 1. Gametophyte development. Sex Plant Reprod 13:61–74

    Article  Google Scholar 

  • Pacini E, Franchi GG (1993) Role of the tapetum in pollen and spore dispersal. Plant Syst Evol [Suppl] 7:1–11

    Google Scholar 

  • Pennell RI, Bell PR (1986) The development of the male gametophyte and spermatogenesis in Taxus baccata L. Proc R Soc London B 228:85–96

    Google Scholar 

  • Reynolds SE (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    CAS  Google Scholar 

  • Roland JB, Vian B (1991) General preparation and staining of thin sections. In: Hall JD, Hawes C (eds) Electron microscopy of plant cells. Academic Press, London, pp 1–66

  • Rowley JR, Walles B (1985a) Cell differentiation in microsporangia of Pinus sylvestris. II. Early pachytene. Nord J Bot 5:241–254

    Google Scholar 

  • Rowley JR, Walles B (1985b) Cell differentiation in microsporangia of Pinus sylvestris. III. Late pachytene. Nord J Bot 5:255–271

    Google Scholar 

  • Rowley JR, Walles B (1987) Origin and structure of Ubisch bodies in Pinus sylvestris. Acta Soc Bot Pol 56:215–227

    Google Scholar 

  • Rowley JR, Walles B (1988) Cell differentiation in microsporangia of Pinus sylvestris: diplotene and the diffuse stage. Ann Sci Nat Bot Paris 13:1–28

    Google Scholar 

  • Rutledge R (1998) Producing sterile trees. Plant Biol Inst Bull May:16–18

    Google Scholar 

  • Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimations of pollen developmental stage and the most sensitive stage to coolness. Proc Crop Sci Soc Japan 39:468–473

    Google Scholar 

  • Satake T, Nishiyama NI, Hayase H (1969) Male sterility caused by cooling treatment at the meiotic stage in rice plants. I. Methods of growing rice plants and inducing sterility in the phytotron. Proc Crop Sci Soc Japan 38:603–608

    Google Scholar 

  • Slobodnik B, Guttenberger H (2000) Ovule, megaspore and female megagametophyte formation in Larix decidua Mill (Pinaceae). Acta Biol Cracov Ser Bot 42:93–100

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    CAS  PubMed  Google Scholar 

  • Strauss SH, Howe GT, Goldfarb B (1991) Prospects for genetic engineering of insect resistance in forest trees. For Ecol Manage 43:181–209

    Google Scholar 

  • Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breeding 1:5–26

    CAS  Google Scholar 

  • Taira H (2000) Characteristics and inheritance of male sterility of Cryptomeria japonica. Proceedings of the XXI IUFRO World Congress. Forests and Society. Role of Research. 7–12 August 2000, Kuala Lumpur, Malaysia

  • Tandre K, Svenson M, Svensson ME, Engstrom P (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J 15:615–623

    Article  CAS  PubMed  Google Scholar 

  • Walden AR, Walter C, Gardner RC (1999) Genes expressed in Pinus radiata male cones include homologs to anther-specific and pathogenesis response genes. Plant Physiol 121:1103–1116

    Article  CAS  PubMed  Google Scholar 

  • Walles B, Rowley JR (1982) Cell differentiation in microsporangia of Pinus sylvestris with special attention to the tapetum. I. The pre- and early-meiotic periods. Nord J Bot 2:53–70

    Google Scholar 

  • Wilson VR, Owens JN (1999) The reproductive biology of totara (Podocarpus totara) (Podocarpaceae). Ann Bot 83:401–411

    Article  Google Scholar 

  • Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY 1 (MS1) gene is a transcription regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39

    Google Scholar 

Download references

Acknowledgements

This study was supported by a National Science and Engineering Research Council grant to J. Owens (grant A1982). Thanks to British Columbia Ministry of Forests staff for access to the Saanich Seed Orchard. Thanks also to two anonymous reviewers, Dr. M. Kainz and L. Malmkvist for review of manuscript content.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vivienne R. Wilson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilson, V.R., Owens, J.N. Histology of sterile male and female cones in Pinus monticola (western white pine). Sex Plant Reprod 15, 301–310 (2003). https://doi.org/10.1007/s00497-003-0166-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-003-0166-8

Keywords

Navigation