Physiological and Proteomic Responses of Rice Peduncles to Drought Stress

Abstract

Panicle exsertion, an essential physiological process for obtaining high grain yield in rice is mainly driven by peduncle (uppermost internode) elongation. Drought at heading/panicle emergence prevented peduncle elongation from reaching its maximum length even after re-watering. This inhibitory effect of drought resulted in delayed heading and trapping spikelets lower down the panicle inside the flag-leaf sheath, thus increasing sterility in the lower un-exserted spikelets and also among the upper superior spikelets whose exsertion was delayed. Intermittent drought stress caused a significant reduction in relative water content (RWC) and an increase in the abscisic acid (ABA) level of the peduncles, while both returned to normal levels upon re-watering. Semi-quantitative reverse transcription polymerase chain reaction (RT-PCR) analysis revealed the down-regulation of GA biosynthetic genes during drought. 2D-PAGE analysis of proteins from peduncles collected under well-watered, drought-stressed, and re-watered plants revealed at least twofold differential changes in expression of 31 proteins in response to drought and most of these changes were largely reversed by re-watering. The results indicate that ABA-GA antagonism is a key focal point for understanding the failure of panicle exsertion under drought stress and the consequent increase in spikelet sterility.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

ABA:

Abscisic acid

GA:

Gibberellic acid

HPLC:

High-performance liquid chromatography

2D-PAGE:

Two-dimensional polyacrylamide gel electrophoresis

MALDI-TOF:

Matrix-assisted laser desorption/ionization-time of flight

RT-PCR:

Reverse transcription polymerase chain reaction

RWC:

Relative water content

References

  1. 1.

    Dey, M. M., & Upadhyaya, H. K. (1996). Yield loss due to drought, cold and submergence in Asia. In R. E. Evenson, R. W. Herdt, & M. Hossain (Eds.), Rice research in Asia: Progress and priorities (pp. 291–303). Wallingford: CAB International.

    Google Scholar 

  2. 2.

    Herdt, R. W. (1991). Research priorities for rice biotechnology. In G. S. Khush & G. H. Toenniessen (Eds.), Rice biotechnology (pp. 19–54). Wallingford: CAB International.

    Google Scholar 

  3. 3.

    Lin, J. Y., & Shen, M. (1993). Rice production constraints in China. In R. E. Everson (Ed.), Rice production in Asia: Progress and priorities (pp. 161–178). Wallingford: CAB International.

    Google Scholar 

  4. 4.

    O’Toole, J. C., & Chang, T. T. (1979). Drought resistance in cereals—rice: A case study. In H. Mussell & R. C. Staples (Eds.), Physiology of crop plants (pp. 374–405). New York: Wiley.

    Google Scholar 

  5. 5.

    Liu, J. X., Liao, D. Q., Oane, R., Estenor, L., Yang, X. E., Li, Z. C., et al. (2006). Genetic variation in the sensitivity of anther dehiscence to drought stress in rice. Field Crops Research, 97, 87–100.

    Article  Google Scholar 

  6. 6.

    O’Toole, J. C., & Namuco, O. S. (1983). Role of panicle exsertion in water stress induced sterility. Crop Science, 23, 1093–1097.

    Article  Google Scholar 

  7. 7.

    Ekanayake, I. J., De Datta, S. K., & Steponkus, P. L. (1989). Spikelet sterility and flowering response of rice to water stress at anthesis. Annals of Botany, 63, 257–264.

    Google Scholar 

  8. 8.

    Hsiao, T. C. (1982). The soil plant atmosphere continuum in relation to drought and crop production. In T. T. Chang, G. C. Loresto, J. C. O’Toole, & J. L. Armenta-Soto (Eds.), Drought resistance in crops with emphasis on rice (pp. 39–52). Philippines: International Rice Research Institute.

    Google Scholar 

  9. 9.

    Ekanayake, I. J., Steponkus, P. L., & De Datta, S. K. (1990). Sensitivity of pollination to water deficits at anthesis in upland rice. Crop Science, 30, 310–315.

    Article  Google Scholar 

  10. 10.

    Kende, H., van der Knaap, E., & Cho, H. G. (1998). Deep water rice—a model plant to study stem elongation. Plant Physiology, 118, 1105–1110.

    Article  CAS  Google Scholar 

  11. 11.

    Hattori, Y., Nagai, K., Furukawa, S., Song, X., Kawano, R., Sakakibara, H., et al. (2009). The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature, 460, 1026–1031.

    Article  CAS  Google Scholar 

  12. 12.

    Kucera, B., Cohn, M. A., & Metzger, G. L. (2005). Plant hormone interactions during seed dormancy release and germination. Seed Science Research, 15, 281–307.

    Article  CAS  Google Scholar 

  13. 13.

    Bray, E. A. (1988). Drought- and ABA-induced changes in polypeptide and mRNA accumulation in tomato leaves. Plant Physiology, 88, 1210–1214.

    Article  CAS  Google Scholar 

  14. 14.

    Ji, X. M., Raveendran, M., Oane, R., Ismail, A., Lafitte, R., Bruskiewich, R., et al. (2005). Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering. Plant Molecular Biology, 59, 945–964.

    Article  CAS  Google Scholar 

  15. 15.

    Khan, M. M., & Komatsu, S. (2004). Rice proteomics: Recent developments and analysis of nuclear proteins. Phytochemistry, 65, 1671–1681.

    Article  CAS  Google Scholar 

  16. 16.

    Abbasi, F. M., & Komatsu, S. (2004). A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics, 4, 2072–2081.

    Article  CAS  Google Scholar 

  17. 17.

    Zang, X., & Komatsu, S. (2007). A proteomics approach for identifying osmotic-stress-related proteins in rice. Phytochemistry, 68, 426–437.

    Article  CAS  Google Scholar 

  18. 18.

    Hajheidari, M., Abdollahian-Noghabi, M., Askari, H., Heidari, M., Sadeghian, S. Y., Ober, E. S., et al. (2005). Proteome analysis of sugar beet leaves under drought stress. Proteomics, 5, 950–960.

    Article  CAS  Google Scholar 

  19. 19.

    Aliashgar, D. D., Mayer-Posner, F. J., Askari, H., Zalee, A., & Salekdeh, G. H. (2006). Proteomic responses of rice young panicles to salinity. Proteomics, 6, 6498–6507.

    Article  Google Scholar 

  20. 20.

    Yang, P., Liang, Y., Shen, S., & Kuang, T. (2006). Proteome analysis of rice uppermost internodes at the milky stage. Proteomics, 6, 3330–3338.

    Article  CAS  Google Scholar 

  21. 21.

    Liu JX, Bennett J (2010) Reversible and irreversible drought induced changes in the anther proteome of rice (Oryza sativa L.) genotypes IR64 and Moroberekkan. Molecular Plant. doi: 10.1093/mp/ssq039.

  22. 22.

    Hu, Y., Li, W., Xu, Y., Li, G., Liao, Y., & Fu, F. (2009). Differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves. Journal of Applied Genetics, 50, 213–223.

    Article  CAS  Google Scholar 

  23. 23.

    Barrs, H. D., & Weatherley, P. E. (1962). A reexamination of relative turgidity for estimating the water deficits in leaves. Australian Journal of Biological Science, 15, 413–428.

    Google Scholar 

  24. 24.

    Krochko, J. E., Abrams, G. D., Loewen, M. K., Abrams, S. R., & Cutler, A. (1998). (+)-Abscisic acid 8′-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiology, 118, 849–860.

    Article  CAS  Google Scholar 

  25. 25.

    Sakamoto, T., Miura, K., Itoh, H., Tatsumi, T., Ueguchi-Tanaka, M., Ishiyama, K., et al. (2004). An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiology, 134, 1642–1653.

    Article  CAS  Google Scholar 

  26. 26.

    Jagadish, S. V. K., Muthurajan, R., Oane, R., Wheeler, T. R., Heuer, S., Bennett, J., et al. (2010). Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). Journal of Experimental Botany, 61, 143–156.

    Article  CAS  Google Scholar 

  27. 27.

    Salekdeh, G. H., Siopongco, J., Wade, L. J., Ghareyazie, B., & Bennett, J. (2002). Proteomic analysis of rice leaves during drought stress and recovery. Proteomics, 2, 1131–1145.

    Article  CAS  Google Scholar 

  28. 28.

    Goodwin, T. W., & Mercer, E. I. (1983). Introduction to plant biochemistry (2nd ed.). Oxford: Pergamon Press.

    Google Scholar 

  29. 29.

    Peleman, J., Boerjan, W., Engler, G., Seurinck, J., Botterman, J., Alliotte, T., et al. (1989). Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. Plant Cell, 1, 81–93.

    Article  CAS  Google Scholar 

  30. 30.

    Higuchi, T. (1981). Biosynthesis of lignin. In W. Tanner & F. A. Loewus (Eds.), Encyclopedia of Plant Physiology, New Series, Vol. 13B: Plant Carbohydrates II (pp. 194–224). Berlin: Springer-Verlag.

    Google Scholar 

  31. 31.

    Mathur, M., Satpathy, M., & Sachar, R. C. (1992). Phytohormonal regulation of S-Adenosylmethionine synthetase by gibberellic acid in wheat aleurones. Molecular Cell Research, 1137, 338–348.

    CAS  Google Scholar 

  32. 32.

    Staiger, C. J. (2000). Signaling to the actin cytoskeleton in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 257–288.

    Article  CAS  Google Scholar 

  33. 33.

    Lemichez, E., Wu, J., Sanchez, J. P., Mettouchi, A., Mathur, J., & Chua, N. H. (2001). Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes and Development, 15, 1808–1816.

    Article  CAS  Google Scholar 

  34. 34.

    Volobueva, O. V., Khokhlova, L. P., Velikanov, G. A., & Opanasiuk, O. A. (2001). Actin-regulated water permeability of two transport channels of plasmodesmata in roots of winter wheat cultivars varying in drought resistance. Tsitologiia, 43, 477–482.

    CAS  Google Scholar 

  35. 35.

    Liu, J., Raveendran, M., Mushtaq, R., Xuemei, J., Xiaoe, Y., Bruskiewich, R., et al. (2005). Proteomic analysis of drought-responsiveness in rice: OsADF5. In R. Tuberosa, R. L. Phillips, & M. Gale (Eds.), From the green revolution to the gene revolution. Italy: University of Bologna.

    Google Scholar 

  36. 36.

    Kurepa, J., Walker, J. M., Smalle, J., Gosink, M. M., Davis, S. J., Durham, T. L., et al. (2003). The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis: Accumulation of SUMO1 and -2 conjugates is increased by stress. Journal of Biological Chemistry, 278, 6862–6872.

    Article  CAS  Google Scholar 

  37. 37.

    Lois, L. M., Lima, C. D., & Chua, N. H. (2003). Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell, 15, 1347–1359.

    Article  CAS  Google Scholar 

  38. 38.

    Shih, M., Hoekstra, F. A., & Hsing, Y. (2008). Late embryogenesis abundant proteins. Advances in Botanical Research, 48, 211–255.

    Article  CAS  Google Scholar 

  39. 39.

    Allagulova, C. R., Gimalov, F. R., Shakirova, F. M., & Vakhitov, V. A. (2003). The plant dehydrins: Structure and putative functions. Biochemistry, 68, 945–951.

    CAS  Google Scholar 

  40. 40.

    Koag, M. C., Fenton, R. D., Wilkens, S., & Close, T. J. (2003). The binding of maize DHN1 to lipid vesicles: Gain of structure and lipid specificity. Plant Physiology, 131, 309–316.

    Article  CAS  Google Scholar 

  41. 41.

    Babu, R. C., Zhang, J., Blum, A., Ho, T. H., Wu, R., & Nguyen, H. T. (2004). HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Science, 166, 855–862.

    Article  CAS  Google Scholar 

  42. 42.

    Cheng, Z., Targolli, J., Huang, X., & Wu, R. (2002). Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.). Molecular Breeding, 10, 71–82.

    Article  CAS  Google Scholar 

  43. 43.

    Sivamani, E., Bahieldin, A., Wraith, J. M., Al-Niemi, T., Dyer, W. E., Ho, T. D., et al. (2000). Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Science, 155, 1–9.

    Article  CAS  Google Scholar 

  44. 44.

    Xiao, B., Huang, Y., Tang, N., & Xiong, L. (2007). Over-expression of a LEA gene in rice improves drought resistance under field conditions. Theoretical and Applied Genetics, 115, 35–46.

    Article  CAS  Google Scholar 

  45. 45.

    Shobbar, Z., Oane, R., Gamuyao, R., Palma, J. D., Malboobi, M., Karimzadeh, G., et al. (2008). Abscisic acid regulates gene expression in cortical fiber cells and silica cells of rice shoots. New Phytologist, 178, 68–79.

    Article  CAS  Google Scholar 

  46. 46.

    Groot, S. P. C., Kieliszewska-Rokicka, B., Vermeer, E., & Karssen, C. M. (1988). Gibberellin-induced hydrolysis of endosperm cell walls in gibberellin-deficient tomato seed prior to radicle protrusion. Planta, 174, 500–504.

    Article  CAS  Google Scholar 

  47. 47.

    Carpita, N. C., & Gibeaut, D. M. (1993). Structural models of primary cell walls in flowering plants: Consistency of molecular structure with the physical properties of the walls during growth. The Plant Journal, 3, 1–30.

    Article  CAS  Google Scholar 

  48. 48.

    Cosgrove, D. J. (1999). Enzymes and other agents that enhance cell wall extensibility. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 391–417.

    Article  CAS  Google Scholar 

  49. 49.

    Moore, J. P., Vicre-Gibouinb, M., Farrantc, J. M., & Driouichb, A. (2008). Adaptations of higher plant cell walls to water loss: Drought vs. desiccation. Physiologia Plantarum, 134, 237–245.

    Article  CAS  Google Scholar 

  50. 50.

    Fry, S. C., Smith, R. C., Renwick, K. F., Martin, D. J., Hodge, S. K., & Matthews, K. J. (1992). Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochemical Journal, 282, 821–828.

    CAS  Google Scholar 

Download references

Acknowledgment

The authors are grateful to the Rockefeller Foundation, USA, and Generation Challenge Program for the fellowship awarded to the first author. L. Estenor, W. H. Oane, P. B. Malabanan, F. V. Gulay, and B. A. Enriquez are thanked for technical assistance during the experiment. This research has been facilitated by access to the Australian Proteome Analysis Facility established under the Australian Government’s Major National Research Facilities Program. Bill Hardy from IRRI is thanked for editing the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. V. K. Jagadish.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 205 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Muthurajan, R., Shobbar, ZS., Jagadish, S.V.K. et al. Physiological and Proteomic Responses of Rice Peduncles to Drought Stress. Mol Biotechnol 48, 173–182 (2011). https://doi.org/10.1007/s12033-010-9358-2

Download citation

Keywords

  • Abscisic acid
  • Drought
  • Peduncle
  • Proteomics
  • Rice