Sexual Plant Reproduction

, Volume 18, Issue 2, pp 81–89

A histological comparison of the development of pollen and female gametophytes in fertile and sterile Cryptomeria japonica

  • Yoshihiro Hosoo
  • Eri Yoshii
  • Kenji Negishi
  • Hideaki Taira
Original Article
  • 107 Downloads

Abstract

To determine a possible mechanism causing male and female sterility in Cryptomeria japonica male and female cones were collected from a C. japonica, tree, ShinDai2, that lacks pollen release and fertile seeds and specimens were processed to examine the development of pollen and female gametophytes using light microscopy and field emission scanning electron microscopy. Pre-meiotic development proceeded normally, but the formation of aberrant meiotic products was observed in cones of both sexes. In sterile microsporangia, heterogeneous microspore populations ranging from monads to polyads gave rise to mature pollen grains of non-uniform size. These pollen grains were covered with an amorphous layer and adhered to each other. In addition, they remained in the microsporangia and were not released even after the onset of pollen dissemination from fertile trees. In the ovules of sterile female cones, megaspores with abnormal shapes, numbers, and sizes formed, and the development of female gametophytes was arrested at the free nuclear or archegonium formation stages. These gametophytes collapsed, and no fertile embryo was generated. Results indicate that meiotic defects are important in the sterility mechanism.

Keywords

Cryptomeria japonica Female gametophyte Meiosis Pollen Sterility 

References

  1. Andersson EA (1947) Case of asyndesis in Picea abies. Hereditas 33:301–347CrossRefGoogle Scholar
  2. Bai X, Peirson BN, Dong F, Xue C, Makaroff CA (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 11:417–430CrossRefPubMedGoogle Scholar
  3. Bhatt M, Lister C, Page T, Fransz P, Findlay K, Jones GH, Dickinson HG, Dean C (1999) The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J 19:463–472CrossRefPubMedGoogle Scholar
  4. Bretagnolle F, Thompson JD (1995) Tansley review no 78. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129:1–22CrossRefGoogle Scholar
  5. Chapman GP (1987) The tapetum. Int Rev Cytol 107:111–125CrossRefGoogle Scholar
  6. 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 14:135–142CrossRefGoogle Scholar
  7. Dogra PD (1966) Embryogeny of the Taxodiaceae. Phytomorphology 16:125–141Google Scholar
  8. El Maâtaoui M, Pichot C (2001) Microsporogenesis in the endangered species Cupressus dupreziana A. Camus: evidence for meiotic defects yielding unreduced and abortive pollen. Planta 213:543–549CrossRefPubMedGoogle Scholar
  9. Hashizume H (1962) Initiation and development of flower buds in Cryptomeria japonica. J Jpn Forest Soc 44:312–319Google Scholar
  10. He C, Mascarenhas JP (1999) MEI1, an Arabidopsis gene required for male meiosis: isolation and characterization. Sex Plant Reprod 11:199–207CrossRefGoogle Scholar
  11. Ilarslan H, Horner HT, Palmer RG (1999) Genetics and cytology of a new male-sterile, female-fertile soybean mutant. Crop Sci 39:658–664CrossRefGoogle Scholar
  12. Inoue T, Osatake H (1988) A new drying method of biological specimens of scanning electron microscopy: The t-butyl alcohol freeze-drying method. Arch Histol Cytol 51:53–59PubMedCrossRefGoogle Scholar
  13. Ishizaki T, Koizumi K, Ikemori R, Ishiyama Y, Kushibiki E (1987) Studies of prevalence of Japanese cedar pollinosis among residents in a densely cultivated area. Ann Allergy 58:265–270PubMedGoogle Scholar
  14. Kurmann MH (1990) Exine formation in Cunninghamia lanceolata (Taxodiaceae). Rev Palaeobot Palynol 64:175–179CrossRefGoogle Scholar
  15. Mascarenhas JP (1990) Gene activity during pollen development. Annu Rev Plant Physiol Plant Mol Biol 41:317–338CrossRefGoogle Scholar
  16. Nagao A, Sasaki S, Pharis RP (1989) Cryptomeria japonica. In: Halevy AH (ed) CRC handbook of flowering, vol 6. CRC, Boca Raton, pp 247–269Google Scholar
  17. Nishihata S, Inouye S, Saiga N, Suzuki S, Murayama K, Yokoyama T, Saito Y (1999) Prevalence rate of allergy to Japanese cedar pollen in Tokyo—from field investigation in 1996 by Tokyo Japanese Cedar Pollen Allergy Measurements and Review Committee. Arerugi 48:597–604PubMedGoogle Scholar
  18. Orr-Ewing AL (1977) Female sterility in Douglas fir. Silvae Genet 26:75–77Google Scholar
  19. Pagliarini MS, De Freitas PM, Takayama SY, Batista LAR (1998) An original meiotic mutation in Paspalum regnellii. Sex Plant Reprod 11:17–21CrossRefGoogle Scholar
  20. Runquist EW (1968) Meiotic investigations in Pinus silvestris (L). Hereditas 60:77–128CrossRefGoogle Scholar
  21. Saito M, Taira H, Furuta Y (1998) Cytological and genetical studies on male sterility in Cryptomeria japonica D. Don. J Forest Res 3:167–173CrossRefGoogle Scholar
  22. Sakaguchi M, Inouye S, Taniai M, Ando S, Usui M, Matsuhasi T (1990) Identification of the second major allergen of Japanese cedar pollen. Allergy 45:309–312PubMedCrossRefGoogle Scholar
  23. Schneider H (1981) Plant anatomy and general botany. In: Clark G (ed) The staining procedures, 4th edn. Williams & Wilkins, Baltimore, pp 315–333Google Scholar
  24. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V (2000) The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127:197–207PubMedGoogle Scholar
  25. Sing H, Chatterjee J (1963) A contribution to the life history of Cryptomeria japonica D. Don. Phytomorphology 13:429–445Google Scholar
  26. Sone T, Komiyama N, Shimizu K, Kusakabe T, Morikubo K, Kino K (1994) Cloning and sequencing of cDNA coding for Cry j1, a major allergen of Japanese cedar pollen. Biochem Biophys Res Commun 15:619–625CrossRefGoogle Scholar
  27. Staiger CJ, Cande WZ (1993) Cytoskeletal analysis of maize meiotic mutants. In: Ormrod JC, Francis D (eds) Molecular and cell biology of the plant cell cycle. Kluwer, Dordrecht, pp 157–171Google Scholar
  28. Stelly DM, Peloquin SJ (1985) Screening for 2n female gametophytes, female fertility, and 2x×4x crossability in potatoes (Solanum spp). Am Potato J 62:519–29Google Scholar
  29. Taira H, Saito M, Furuta Y (1999) Inheritance of the trait of male sterility in Cryptomeria japonica. J Forest Res 4:271–273CrossRefGoogle Scholar
  30. Takaso T, Tomlinson PB (1989) Aspects of cone and ovule ontogeny in Cryptomeria (Taxodiaceae). Am J Bot 76:692–705CrossRefGoogle Scholar
  31. Uehara K, Sahashi N (2000) Pollen wall development in Cryptomeria japonica (Taxodiaceae). Grana 39:267–274CrossRefGoogle Scholar
  32. Wilson VR, Owens JN (2003) Histology of sterile male and female cones in Pinus monticola (western white pine). Sex Plant Reprod 15:301–315Google Scholar
  33. 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 28:27–39CrossRefPubMedGoogle Scholar
  34. Wüthrich B (1989) Epidemiology of the allergic diseases: are they really on the increase? Int Arch Allergy Appl Immunol 90:3–10PubMedGoogle Scholar
  35. Wüthrich B, Schindler C, Leuenberger P, Ackermann-Liebrich U (1995) Prevalence of atopy and pollinosis in the adult population of Switzerland (SAPALDIA study). Swiss study on air pollution and lung diseases in adults. Int Arch Allergy Appl Immunol 106:149–156Google Scholar
  36. Yang M, Hu Y, Lodhi M, McCombie WR, Ma H (1999) The Arabidopsis SKP1-LIKE gene is essential for male meiosis and may control homologue separation. Proc Natl Acad Sci USA 96:11416–11421CrossRefPubMedGoogle Scholar
  37. Yasueda H, Yui Y, Shimizu T, Shida T (1983) Isolation and partial characterization of major allergen from Japanese cedar (Cryptomeria japonica) pollen. J Allergy Clin Immunol 71:77–86CrossRefPubMedGoogle Scholar
  38. Yokoyama T (1975) Embryogenesis and cone growth in Cryptomeria japonica. Bull Gov Forest Exp Stn 257:1–20Google Scholar
  39. Yokoyama T (1997) The cause of self-sterilely in Cryptomeria japonica D. Don. J Jpn Forest Soc 59:389–390Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Yoshihiro Hosoo
    • 1
  • Eri Yoshii
    • 2
  • Kenji Negishi
    • 3
  • Hideaki Taira
    • 1
  1. 1.Chair of Climate Change Science for Forestry and Water-Resources, Graduate School of Science and TechnologyNiigata UniversityNiigataJapan
  2. 2.Chair of Ecosystem Science, Graduate School of Science and TechnologyNiigata UniversityNiigataJapan
  3. 3.Department of Production and Environmental Science, Faculty of AgricultureNiigata UniversityNiigataJapan

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