Skip to main content
Log in

Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The tapetum plays a crucial role in pollen development. This secretory tissue produces numerous nutritive proteins necessary for pollen maturation. The tapetum, whose cells undergo programmed cell death (PCD), is completely diminished by the time the pollen is fully mature. Our previous studies on a thermosensitive genic male-sterile (TGMS) rice (Oryza sativa L.) suggested that male-sterility was due to failure in pollen development. In this paper we describe how further analysis of the TGMS rice revealed that male-sterility is associated with premature PCD of the tapetum. Cytological observations of TGMS rice anthers at various developmental stages indicated that PCD initiates at an early stage of pollen development and continues until the tapetal cells are completely degraded, resulting in pollen collapse. Transmission electron microscopy showed the morphologically distinct hallmarks of apoptosis, including cytoplasmic shrinkage, membrane blebbing, and vacuolation. Identification of DNA fragmentation using the TUNEL assay supports the hypothesis that premature PCD is associated with male-sterility in the rice. The tissue-specific feature of the thermosensitive genic male-sterile phenotype is discussed with regard to PCD during anther development.

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.

Institutional subscriptions

Fig. 1a–j.
Fig. 2a, b.
Fig. 3a–d.
Fig. 4a–h.
Fig. 5a–c.

Similar content being viewed by others

Abbreviations

CMS:

cytoplasmic male-sterility

EGMS:

environmental genic male-sterility

PCD:

programmed cell death

TGMS:

thermo-sensitive genic male-sterility

TUNEL:

TdT-mediated dUTP nick-end labelling

References

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    CAS  PubMed  Google Scholar 

  • Bethke PC, Lonsdale JE, Fath A, Jones, RL (1999) Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11:1033–1045

    Article  CAS  PubMed  Google Scholar 

  • Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98:6522–6527

    Article  CAS  PubMed  Google Scholar 

  • Hernould M, Suharsono, Zabaleta E, Carde JP, Litvak S, Araya A, Mouras A (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol Biol 36:499–508

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison J (1976) The adaptive significance of the exine. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic Press, New York, pp 27–38

  • Kapoor S, Kobayashi, A, Takatsuji, H (2002) Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14:2353–2367

    Article  CAS  PubMed  Google Scholar 

  • Kaul M (1988) Male sterility in higher plants, vol 10. Springer, Berlin Heidelberg New York

  • Kofer W, Glimelius K, Bonnett HT (1991) Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 3:759–769

    Article  CAS  PubMed  Google Scholar 

  • Ku S-J, Cho K-H, Choi Y-J, Baek W-K, Kim S, Suh H-S, Chung Y-Y (2001) Cytological observation of two environmental genic male-sterile lines of rice. Mol Cells 12:403–406

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Mackenzie S, Shichuan H, Lyznik A (1994) The elusive plant mitochondrion as a genetic system. Plant Physiol 105:775–780

    CAS  PubMed  Google Scholar 

  • Mariani C, Beuckeleer MD, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347:737–741

    CAS  Google Scholar 

  • Meuter-Gerhards A, Riegart S, Wiermann R (1999) Studies on sporopollenin biosynthesis in Cucurbita maxima (DUCH-II): the involvement of aliphatic metabolism. J. Plant Physiol 154:431–436

    CAS  Google Scholar 

  • Mittler R, Lam E (1996) Sacrifice in the face of foes: pathogen-induced programmed cell death. Trends Microbiol 4:10–15

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Feng X, Cohen M (1998) Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10:461–473

    Google Scholar 

  • Paxson-Sowders DJ, Dodrill CJ, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127:1739–1749

    Google Scholar 

  • Rozema J, Croekman RA, Blokker P, Meijkamp BB, de Bakker N, van de Staaij J, van Beem A, Ariese F, Kars SM (2001) UV-B absorbance and UV-B absorbing compounds (para-coumaric acid) in pollen and sporopollenin: the perspective to track historic UV-B levels. J Photochem Photobiol B 62:108–117

    Article  CAS  PubMed  Google Scholar 

  • Schnabel PS, Wise RP (1998) The molecular basis of cytoplasmic male-sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Stanley RG, Linskens HF (1974) Pollen: biology, biochemistry, management. Springer, Berlin Heidelberg New York, pp 13–28

  • Van der Meer IM, Stam ME, van Tunen AJ, Mol JNM, Stuitje AR (1992) Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4:253–262

    Article  PubMed  Google Scholar 

  • Wang M, Hoekstra S, van Bergen S, Lamers GEM, Oppedijk BJ, van der Heijden MW, de Priester W, Schilperoort RA (1999) Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L. Plant Mol Biol 39:489–501

    CAS  PubMed  Google Scholar 

  • Xu Y, Hanson MR (2000) Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol 122:1323–1333

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Center for Plant Molecular Genetics and Breeding Research, Korea Science and Engineering Foundation. We acknowledge the Wild Crop Germplasm Bank of Yeungnam University for providing the TGMS rice used in this study. We also thank Dr. Martin B. Dickman of the University of Nebraska for his comments regarding this manuscript and Sanghyun Lee for his helps in preparing figures. S. Ku and H. Yoon contributed equally to this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong-Yoon Chung.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ku, S., Yoon, H., Suh, H.S. et al. Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217, 559–565 (2003). https://doi.org/10.1007/s00425-003-1030-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1030-7

Keywords

Navigation