Photosynthetica, 2009 (vol. 47), issue 4

Photosynthetica 2009, 47(4):536-547 | DOI: 10.1007/s11099-009-0079-3

Wheat cultivars differing in heat tolerance show a differential response to monocarpic senescence under high-temperature stress and the involvement of serine proteases

S. Chauhan1, S. Srivalli1, A. R. Nautiyal2, R. Khanna-Chopra1,*
1 Stress Physiology Laboratory, Water Technology Centre, Indian Agricultural Research Institute, New Delhi, India
2 High Altitude Plant Physiology Research Centre, H.N.B. Garhwal University, Srinagar, Uttarakhand, India

High temperature is a common constraint during anthesis and grain-filling stages of wheat leading to huge losses in yield. In order to understand the mechanism of heat tolerance during monocarpic senescence, the present study was carried out under field conditions by allowing two well characterized Triticum aestivum L. cultivars differing in heat tolerance, Hindi62 (heat-tolerant) and PBW343 (heat-susceptible), to suffer maximum heat stress under late sown conditions. Senescence was characterized by measuring photosynthesis related processes and endoproteolytic activity during non-stress environment (NSE) as well as heat-stress environment (HSE). There was a faster rate of senescence under HSE in both the genotypes. Hindi62, having pale yellow flag leaf with larger area, maintained cooler canopy under high temperatures than PBW343. The tolerance for high temperature in Hindi62 was clearly evident in terms of slower green-leaf area degradation, higher stomatal conductance, higher stability in maximum PSII efficiency, Rubisco activity and Rubisco content than PBW343. Both the genotypes exhibited lower endopeptidase activity under HSE as compared to NSE and this difference was more apparent in Hindi62. Serine proteases are the predominant proteases responsible for protein degradation under NSE as well as HSE. Flag leaf of both the genotypes exhibited high-molecular-mass endoproteases (78 kDa and 67 kDa) isoforms up to full grain maturity which were inhibited by specific serine protease inhibitor in both the environments. In conclusion, the heat-tolerant Hindi62 exhibited a slower rate of senescence than the heat-susceptible PBW343 during HSE, which may contribute towards heat stability.

Keywords: heat stress; photosynthesis; Rubisco; senescence; serine protease; wheat

Received: October 14, 2008; Accepted: September 29, 2009; Published: December 1, 2009Show citation

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Chauhan, S., Srivalli, S., Nautiyal, A.R., & Khanna-Chopra, R. (2009). Wheat cultivars differing in heat tolerance show a differential response to monocarpic senescence under high-temperature stress and the involvement of serine proteases. Photosynthetica, 47(4), 536-547. doi: 10.1007/s11099-009-0079-3.
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    References

    1. Aggarwal, P.K., Sinha, S.K.: Performance of wheat and tritcale varieties in a variable soil water environment. IV. Yield components and their association with grain yield. - Field Crops Res. 17: 45-53, 1987. Go to original source...
    2. Al-Khatib, K., Paulsen, G.M.: Mode of high-temperature injury to wheat during grain development. - Physiol. Plant. 61: 363-368, 1984. Go to original source...
    3. Benbella, M., Paulsen, G.M.: Efficacy of treatments for delaying senescence of wheat leaves: II. Senescence and grain yield under field conditions. - Agron. J. 90: 332-338, 1998. Go to original source...
    4. Berry, J., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants. - Ann. Rev. Plant Physiol. 31: 491-543, 1980. Go to original source...
    5. Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T., Pink, D.: The molecular analysis of leaf senescence - a genomics approach - Plant Biotechnol. J. 1: 3-22, 2003. Go to original source...
    6. CIMMYT.: CIMMYT/NARS Consultancy on ME1 bread wheat breeding. - Wheat special report No. 38. Mexico, DF 1995.
    7. Demmig-Adams, B., Adams, W.W., III.: Photoprotection and other responses of plants to high light stress. - Ann. Rev. Plant Physiol. 43: 599-626, 1992.
    8. Distefano, S., Palma, J.M., Gomez, M., del Rio, L.A.: Characterization of endoproteases from plant peroxisomes. - Biochem. J. 327: 399-405, 1997. Go to original source...
    9. Ferreira, L.C.S., Bressan-Smith, R., Elias, T.F., Silva, F.F., Viana, L.H., Oliveira J. G.: Short-term responces of photosynthetic membrane lipids and photochemical effienciency in plants of Phaseolus vulgaris and Vigna unguiculata submitted to high irradiance. - Photosynthetica 45: 23-29, 2007. Go to original source...
    10. Ferris, R., Ellis, R.H., Wheeeler, T.R., Hadley, P.: Effect of high temperature stress at anthesis on grain yield and biomass of field grown crops of wheat. - Plant Cell Environ. 34: 67-78, 1998. Go to original source...
    11. Gilmore, A.M.: Mechanistic aspect of xanthophylls cycledependent photoprotection in higher plant chloroplast and leaves. - Physiol. Plant. 99: 197-209, 1997. Go to original source...
    12. Gregersen, P.L., Holm, P.B.: Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). - Plant Biotechnol. J. 5: 192-206, 2007. Go to original source...
    13. Guo, Y., Cai, Z., Gan, S.: Transcriptome of Arabidopsis leaf senescence. - Plant Cell Environ. 27: 521-549, 2004. Go to original source...
    14. Hebeler, R., Oeljeklaus, S., Reidegeld, K.A., Eisenacher, M., Stephan, C., Sitek, B., Stühler, K., Meyer, H.E., Sturre, M.J.G., Dijkwel, P.P., Warscheid, B.: Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14N/15N labeling and difference gel electrophoresis. - Mol. Cell. Proteom. 7: 108-120, 2008.
    15. Jiang, C.Z., Rodermel, S.R. Shibles, R.M.: Photosynthesis, rubisco activity and amount, and their regulation by transcription in senescing soybean leaves. - Plant Physiol. 101: 105-112, 1993. Go to original source...
    16. Laemmli, U.K.: Cleavage of structure proteins during the assembly of the head of bacteriophage T4. - Nature 227: 680-685, 1970. Go to original source...
    17. Law, R.D., Crafts-Brandner, S.J.: Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. - Plant Physiol. 120: 173-181, 1999. Go to original source...
    18. Lichtenthaler, H.K.: Chlorophylls and carotenoids: Pigments of 382, 1987.
    19. Lim, P.O., Kim, H.J., Nam, H.G.: Leaf senescence. - Annu. Rev. Plant Biol. 58: 115-136, 2007. Go to original source...
    20. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the Folin-phenol reagent. - J. Biol. Chem. 193: 265-275, 1951.
    21. Mae, T., Kamei, C., Funaki, K., Miyadai, K., Makino, A., Ohira, K., Ojima, K.: Degradation of ribulose-1,5-bisphosphate carboxylase oxygenase in the lysate of the chloroplasts isolated mechanically from wheat (Triticum aestivum L.) leaves. - Plant Cell Physiol. 30: 193-200, 1989. Go to original source...
    22. Martínez, D.E., Bartoli, C.G., Grbic, V., Guiamet, J.J.: Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. - J. Exp. Bot. 58: 1099-1107, 2007. Go to original source...
    23. Morales, D., Rodríguez, P., Dell'Amico, J., Nicolás, E., Torrecillas, A., Sánchez-Blanco, M.J.: High-temperature preconditioning and thermal shock imposition affects water relations, gas exchange and root hydraulic conductivity in tomato. - Biol. Plant. 47: 203-208, 2003.
    24. Moreno, J., Penarubbia, L., Garcia-Ferris, C.: The mechanism of redox regulation of ribulose-1,5-bisphosphate carboxylase oxygenase turnover - a hypothesis. - Plant Physiol. Biochem. 33: 121-127, 1995.
    25. Mullarkey, M., Jones, P.: Isolation and analysis of thermotolerant mutants of wheat. - J. Exp. Bot. 51: 139-146, 2000. Go to original source...
    26. Noodén, L.D.: The phenomenon of senescence and aging. - In: Noodén, L.D., Leopold, A.C. (ed.): Senescence and Aging in Plants. Pp. 1-50. Academic Press Inc., New York 1988. Go to original source...
    27. Patil, R.V., Chinnusamy, V., Chauhan, S., Ruwali, K.N., Pandey, H.N., Khanna-Chopra, R.: Heat stress tolerance in T. aestivum and T. durum wheat genotypes under continual and terminal heat stress environments. - J. Plant Biol. 35: 1-10, 2007.
    28. Paulsen, G.M..: High temperature responses of crop plants. - In: Boote, K.J., Bennet, J.M., Sinclair, T.R., Paulsen, G.M. (ed.): Physiology and Determination of Crop Yield. Pp. 365-389. ASA-CSSA-SSSA, Madion 1994.
    29. Peoples, M.B., Dalling, M.J.: The interplay between the proteolysis and amino acid metabolism during senescence and nitrogen reallocation. - In: Noodén, L.D., Leopold, A.C. (ed.): Senescence and aging in plants. Pp. 181-217. Academic Press Inc., New York 1988. Go to original source...
    30. Peoples, M.B., Pate, J.S., Atkins, C.A.: Mobilization of nitrogen in fruiting plants of a cultivar of cowpea. - J. Exp. Bot. 34: 563-578, 1983. Go to original source...
    31. Plaut, Z., Butow, B.J., Blumenthal, C.S., Wrigley, C.W.: Transport of dry matter into developing wheat kernels and its contribution to grain yield under post-anthesis water deficit and elevated temperature. - Field Crops Res. 86: 185-198, 2004. Go to original source...
    32. Porter, J.R., Gawith, M.: Temperatures and the growth and development of wheat: a review. - Eur. J. Agron. 10: 23-36, 1999. Go to original source...
    33. Porter, J.R.: Rising temperatures are likely to reduce crop yields. - Nature 436: 174-174, 2005. Go to original source...
    34. Reynolds, M.P., Balota, M., Delgado, M.I.B., Amani, I., Fisher, R.A.: Physiological and morphological traits associated with spring wheat yield under hot, irrigated conditions. - Aust. J. Plant Physiol. 21: 717-730, 1994. Go to original source...
    35. Reynolds, M.P., Delgado, M.I.B., Gutiérrez-Rodríguez, M., Larqué-Saavedra, A.: Photosynthesis of wheat in a warm, irrigated environment. I. Genetic diversity and crop productivity. - Field Crops Res. 66: 37-50, 2000. Go to original source...
    36. Roberts, I.N., Murray, P.F., Caputo, C.P., Passeron, S., Barneix, A.J.: Purification and characerization of a substilisin-like serine protease induced during the senescence of wheat leaves. - Physiol. Plant. 118: 483-490, 2003. Go to original source...
    37. Roberts, I.N., Passeron, S., Barneix, A.J.: The two main endoproteases present in dark-induced senescent wheat leaves are distinct subtilisin-like proteases. - Planta 224:1437-1447, 2006. Go to original source...
    38. Ruwali, K.N., Prasad, L.: Effect of temperature stress on yield production of wheat. - In: Proc. Int. Conf. Plant Physiol. Pp. 271-277. BHU, India, Varanasi 1991.
    39. Salvucci, M.E., Crafts-Brandner, S.J.: Inhibition of photosynthesis by heat stress: The activation state of Rubisco as a limiting factor in photosynthesis. - Physiol. Plant. 120: 179-186, 2004. Go to original source...
    40. Schippers, J.H.M., Jing, H.C., Hille, J., Dijkwel, P.P.: Developmental and hormonal control of leaf senescence. - In: Gan, S. (ed.): Senescence Processes in Plants. Pp. 145-170. Blackwell Publishing, Oxford 2007. Go to original source...
    41. Schreiber, U., Bilger, W., Neubauer, C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. - In: Schulze, E.-D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis, Pp. 49-70. Springer-Verlag, Berlin 1994. Go to original source...
    42. Sharkova, V.E.: The effect of heat shock on the capacity of wheat plants to restore their photosynthetic electron transport after photoinhibition or repeated heating. - Russ. J. Plant Physiol. 48: 793-797, 2001. Go to original source...
    43. Sinha, S.K., Singh, G.B., Rai, M.: Decline in crop productivity in Haryana and Punjab: Myth or Reality? - Report of the fact finding committee, ICAR, India, New Delhi 1998.
    44. Smart, C.M.: Gene expression during leaf senescence. - New Phytol. 126: 419-448, 1994. Go to original source...
    45. Srivalli, B., Khanna-Chopra, R.: Flag leaf senescence in relation to reduced reproductive sink strength in wheat. - Ind. J. Exp. Biol. 36: 1013-1019, 1998.
    46. Srivalli, B., Bharti, S., Khanna-Chopra, R.: Vacuolar cysteine proteases and ribulose-1,5-bisphosphate carboxylase/oxygenase degradation during monocarpic senescence in cowpea leaves. - Photosynthetica 39: 87-93, 2001. Go to original source...
    47. Tewolde, H., Fernandez, C.J., Erickson, C.A., Wheat cultivars adapted to post-heading high temperature stress. - J. Agron. Crop Sci. 192: 111-120, 2006. Go to original source...
    48. Towbin, H., Staehelin, T., Gorgon, J.: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some application. - Proc. Natl. Acad. Sci. USA 76: 4350-4354, 1979. Go to original source...
    49. Viswanathan, C., Khanna-Chopra, R.: Heat shock proteins - Role in thermotolerance of crop plants. - Curr. Sci. 71: 275-284, 1996.
    50. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: An overview. - Environ. Exp. Bot. 61: 199-223, 2007. Go to original source...
    51. Wardlaw, I.F., Wrigley, C.W.: Heat tolerance in temperate cereals - an overview. - Aust. J. Plant Physiol. 21: 695-703, 1994. Go to original source...
    52. Ye, Z.H., Varner, J.E.: Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans. - Plant Mol. Biol. 30: 1233-1246, 1996. Go to original source...
    53. Zaharieva, M., Gaulin, E., Havaux, M., Acevedo, E., Monneveux, P.: Drought and heat responses in the wild wheat relative Aegilops geniculata Roth: Potential interest for wheat improvement. - Crop Sci. 41: 1321-1329, 2001. Go to original source...
    54. Zhong-Hu, H., Rajaram, S.: Differential responses of bread wheat characters to high temperature. - Euphytica 72: 197-203, 1993.
    55. Zhang, L.-F., Rui, Q., Zhang, P., Wang, X.-Y., Xu, L.-L.: A novel 51-kDa fragment of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase formed in the stroma of chloroplasts in dark-induced senescing wheat leaves. - Physiol. Plant. 131: 64-71, 2007. Go to original source...
    56. Zhao, H., Dai, T.B., Jing, Q., Jiang, D., Cao, W.X.: Leaf senescence and grain filling affected by post-anthesis high temperatures in two different wheat cultivars. - Plant Growth Regul. 51: 149-158, 2007. Go to original source...
    57. Zivy, M., Thiellement, H., Devienne, D., Hofmann, J.P.: Study on molecular and cytoplasmic genome expression in wheat by two-dimensional gel electrophoresis. 1. 1st results on 18 alloplasmic lines. - Theor. Appl. Genet. 66: 1-7, 1983. Go to original source...

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