Skip to main content
SpringerLink
Log in

Ultrastructural study of rice tapetum under low-temperature stress

  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The development of male reproductive organs in rice is very sensitive to various environmental stresses. For example, exposing plants to low temperatures during the heading stage leads to a reduction in grain yield. Here, we grew rice under normal conditions and also at three different temperatures -- 16, 18, and 20°C. Treatment at a low temperature significantly decreased pollen viability and grain production. Cytological observations of the anther showed that the tapetum was the most sensitive to low-temperature stress, resulting in male sterility due to functional loss of the tissue. Detailed observations by transmission electron microscopy suggested that this abnormality was restricted primarily to the ER structures. The endoplasmic reticulum, a highly vulnerable sub-cellular organelle, showed two typical morphological aberrations, one in its pattern of arrangement, the other in the formation of ER bodies. Of our three experimental chilling temperatures, the most severe abnormalities were observed in tapetal cells exposed to 16°C.

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

Similar content being viewed by others

Literature Cited

  • Angus JF, Lewin LG (1991) Forecasting Australian rice yields,In S Cheng, CW Cady, eds, Climatic Variation and Change: Implications for the Pacific Rim. University of California, Davis, pp 1–8

    Google Scholar 

  • Belanger FC, Brodl MR, Ho TD (1986) Heat shock causes destabilization of specific mRNAs and destruction of endoplasmic reticulum in barley aleurone cells. Proc Natl Acad Sci USA83: 1354–1358

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS, Westgate ME (2004) Grain yields with limited water. J Exp Bot55: 2385–2394

    Article  PubMed  CAS  Google Scholar 

  • Chaudhury A (1993) Nuclear genes controlling male fertility. Plant Cell5: 1277–1283

    Article  PubMed  Google Scholar 

  • Chrispeels MJ, Greenwood JS (1987) Heat stress enhances phyto- hemagglutinin synthesis but inhibits its transport out of the endoplasmic reticulum. Plant Physiol83: 778–784

    Article  PubMed  CAS  Google Scholar 

  • Ciampolini F, Shibvanna KR, Cristi M (1991) High humidity and heat stress cause dissociation of endoplasmic reticulum in tobacco pollen. Bot Acta104: 110–116

    Google Scholar 

  • Clement C, Audran JC (1995) Anther wall layers control pollen sugar nutrition inLilium. Protoplasma187: 172–181

    Article  CAS  Google Scholar 

  • Clement C, Chavant L, Burrus M, Audran JC (1994) Anther starch variations inLilium during pollen development. Sex Plant Reprod7: 347–356

    Article  Google Scholar 

  • Clement C, Laporte R, Audran JC (1998) The loculus content and tapetum during pollen development inLilium. Sex Plant Reprod11: 94–106

    Article  Google Scholar 

  • Fei H, Sawhney VK (1999) MS32 regulated timing of callose degradation during microsporogenesis inArabidopsis is associated with the accumulation of stacked rough ER in tapetal cells. Sex Plant Reprod12: 188–193

    Article  CAS  Google Scholar 

  • Hara-Nishimura I, Matsushima R (2003) A wound inducible organelle derived from endoplasmic reticulum: A plant strategy against environmental stresses? Curr Opin Plant Biol6: 583–588

    Article  PubMed  CAS  Google Scholar 

  • Harris N (1986) Organization of the endomembrane system. Annu Rev Plant Physiol37: 73–92

    Article  CAS  Google Scholar 

  • Hauser BA, Sun K, Oppenheimer DG, Sage TL (2005) Changes in mitochondrial membrane potential and accumulation of reactive oxygen species precede ultrastructural changes during ovule abortion. Planta223: 492–499

    Article  PubMed  CAS  Google Scholar 

  • Hayase H, Satake T, Nishiyama I, Ito N (1969) Male sterility caused by cooling treatment at the meiotic stage in rice plants: II. The most sensitive stage to cooling and the fertilising ability of pistils. Proc Crop Sci Soc Jpn38: 706–711

    Google Scholar 

  • Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development inArabidopsis thaliana. Plant J35: 177–192

    Article  PubMed  CAS  Google Scholar 

  • Imin N, Kerim T, Weinman JJ, Rolfe BG (2006) Low temperature treatment at the young microspore stage induces protein changes in rice anthers. Mol Cell Proteom5: 274–292

    Article  CAS  Google Scholar 

  • Ito N, Hayase H, Satake T, Nishiyama I (1970) Male sterility caused by cooling treatment at the meiotic stage in rice plants: III. Male abnormalities at anthesis. Proc Crop Sci Soc Jpn39: 60–64

    Google Scholar 

  • Jacobs BC, Pearson CJ (1994) Cold damage and development of rice: A conceptual model. Aust J Exp Agric34: 917–919

    Article  Google Scholar 

  • Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice undeveloped tapetum1 is a major regulator of early tapetum development. Plant Cell17: 2705–2722

    Article  PubMed  CAS  Google Scholar 

  • Kandasamy MK, Kristen U (1989) Ultrastructural responses of tobacco pollen tubes to heat shock. Protoplasma153: 104–110

    Article  Google Scholar 

  • 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 Cell14: 2353–2367

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi K, Shibuya N, Ishii T (1996) A novel tetrasaccharide, with a structure similar to the terminal sequence of an arabinogalactan protein, accumulates in rice anthers in a stagespecific manner. Plant J9: 777–785

    Article  PubMed  CAS  Google Scholar 

  • Ku SJ, Cho KH, Choi YJ, Baek WK, Kim S, Suh HS, Chung YY (2001) Cytological observation of two environmental genic male-sterile lines of rice. Mol Cell12: 403–406

    CAS  Google Scholar 

  • Ku SJ, Yoon HJ, Suh HS, Chung YY (2003) Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta217: 559–565

    Article  PubMed  CAS  Google Scholar 

  • Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int30: 583–591

    Article  PubMed  CAS  Google Scholar 

  • Mamun EA, Cantrill LC, Overall RL, Sutton BG (2005) Cellular organization in meiotic and early post-meiotic rice anthers. Cell Biol Int29: 903–913

    Article  PubMed  CAS  Google Scholar 

  • Matsushima R, Kondo M, Nishimura M, Hara-Nishimura I (2003) A novel ER-derived compartment, the ER body, selectively accumulates a b glucosidase with an ER-retention signal inArabidopsis. Plant J33: 493–502

    Article  PubMed  CAS  Google Scholar 

  • Morisset C (1983) Effects of energetic shortage upon the ultrastructure of some organelles in excised roots ofLycopersicum esculentum cultivatedin vitro: I. Reversible structural modifications of the endoplasmic reticulum. Cytologia48: 349–362

    Google Scholar 

  • Nishiyama I (1984) Climatic influence on pollen formation and fertilization,In S Tsunoda, N Takahashi, eds, Biology of Rice. Japan Scientific Societies Press, Tokyo, pp 153–171

    Google Scholar 

  • Nishiyama I (1995) Physiological basis of the damage caused by unfavorable climatic conditions, diseases and insect pests,In T Matsuo, K Kumazawa, R Ishii, H Ishihara, H Hirata, eds, Science of the Rice Plant. Food and Agriculture Policy Research Center, Tokyo, pp 769–793

    Google Scholar 

  • Oliver SN, Dongen JV, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ28: 1534–1551

    Article  CAS  Google Scholar 

  • Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis inArabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma185: 7–21

    Article  Google Scholar 

  • Pacini E, Franchi GG (1983) Pollen grain development inSmilax aspera L. and possible functions of the loculus,In DL Mulcahy, E Ottaviano, eds, Pollen Biology and Implications for Plant Breeding. Elsevier Biomedical, New York, pp 183–190

    Google Scholar 

  • Pacini E, Franchi GG, Hesse M (1985) The tapetum: Its form, function, and possible phylogeny inEmbryophyta. Plant Syst Evol149: 155–185

    Article  Google Scholar 

  • Platt KA, Huang AHC, Thomson WW (1998) Ultrastructural study of lipid accumulation in tapetal cells ofBrassica napus L. cv. Westar during microsporogenesis. Intl J Plant Sci159: 724–737

    Article  CAS  Google Scholar 

  • Raghavan V (1988) Anther and pollen development in rice (Oryza sativa). Amer J Bot75: 183–186

    Article  Google Scholar 

  • Saini HS, Westgate ME (2000) Reproductive development in grain crops during drought. Adv Agron68: 59–96

    Article  Google Scholar 

  • Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants: V. Estimation of pollen developmental stage and the most sensitive stage to coolness. Proc Crop Sci Soc Jpn39: 468–473

    Google Scholar 

  • Satake T, Hayase H (1974) Male sterility caused by cooling treatment at the young microspore stage in rice plants: IX. Revision of the classification and terminology of pollen developmental stages. Proc Crop Sci Soc Jpn43: 36–39

    Google Scholar 

  • Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice - changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod9: 161–169

    Article  Google Scholar 

  • Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen inArabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J29: 581–594

    Article  PubMed  CAS  Google Scholar 

  • Sorensen AM, Krober S, Unte US, Huijser R Dekker K, Saedler H (2003) TheArabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J33: 413–423

    Article  PubMed  CAS  Google Scholar 

  • Steer MW (1977) Differentiation of the tapetum in Avena: II. The endoplasmic reticulum and Golgi apparatus. J Cell Sci28: 71–86

    PubMed  CAS  Google Scholar 

  • Suzuki K, Takeda H, Tsukaguchi T, Egawa Y (2001) Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. Sex Plant Reprod13: 293–299

    Article  Google Scholar 

  • Vitale A, Ceriotti A, Denecke J (1993) The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J Exp Bot44: 1417–1444

    Article  CAS  Google Scholar 

  • Wada T, Ogawa K, Ito T, Suzuki H, Takeoka Y (1990) Light microscopic observations on pollen and anther development in rice (Oryza sativa L.): I. Stages from pollen mother cells to tetrads. Jpn J Crop Sci59: 769–777

    Google Scholar 

  • Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) TheArabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD- finger family of transcription factors. Plant J28: 27–39

    Article  PubMed  CAS  Google Scholar 

  • Wi SZ, Chung BY, Kim JH, Baek MH, Yang DH, Lee JW Kim JS (2005) Ultrastrutural changes of cell organelles inArabidopsis stem after gamma irradiation. J Plant Biol48: 195–200

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Life Sciences and Biotechnology, Korea University, 136-701, Seoul, Korea

    Kodiveri Muthukaliannan Gothandam, Eun Sook Kim & Yong Yoon Chung

  2. School of Biotechnology, Chemical and Biomedical Engineering, Vellore Institute of Technology, Vellore, 632 014, Tamil Nadu, India

    Kodiveri Muthukaliannan Gothandam

Authors
  1. Kodiveri Muthukaliannan Gothandam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eun Sook Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong Yoon Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yong Yoon Chung.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gothandam, K.M., Kim, E.S. & Chung, Y.Y. Ultrastructural study of rice tapetum under low-temperature stress. J. Plant Biol. 50, 396–402 (2007). https://doi.org/10.1007/BF03030674

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03030674

Keywords

Search

Navigation