Photosynthetica 2013, 51(1):85-94 | DOI: 10.1007/s11099-013-0001-x

Study of the senescence process in primary leaves of sunflower (Helianthus annuus L.) plants under two different light intensities

L. De La Mata1, P. Cabello1, P. De La Haba1, E. Agüera1,*
1 Departamento de Botánica, Ecología y Fisiología Vegetal, Área de Fisiología Vegetal, Facultad de Ciencias, Universidad de Córdoba, Córdoba, Spain

Different parameters that vary during leaf development may be affected by light intensity. To study the influence of different light intensities on primary leaf senescence, sunflower (Helianthus annuus L.) plants were grown for 50 days under two photon flux density (PFD) conditions, namely high irradiance (HI) at 350 μmol(photon) m-2 s-1 and low irradiance (LI) at 125 μmol(photon) m-2 s-1. Plants grown under HI exhibited greater specific leaf mass referred to dry mass, leaf area and soluble protein at the beginning of the leaf development. This might have resulted from the increased CO2 fixation rate observed in HI plants, during early development of primary leaves. Chlorophyll a and b contents in HI plants were lower than in LI plants in young leaves. By contrast, the carotenoid content was significantly higher in HI plants. Glucose concentration increased with the leaf age in both treatments (HI and LI), while the starch content decreased sharply in HI plants, but only slightly in LI plants. Glucose contents were higher in HI plants than in LI plants; the differences were statistically significant (p<0.05) mainly at the beginning of the leaf senescence. On the other hand, starch contents were higher in HI plants than in LI plants, throughout the whole leaf development period. Nitrate reductase (NR) activity decreased with leaf ageing in both treatments. However, the NR activation state was higher during early leaf development and decreased more markedly in senescent leaves in plants grown under HI. GS activity also decreased during sunflower leaf ageing under both PFD conditions, but HI plants showed higher GS activities than LI plants. Aminating and deaminating activities of glutamate dehydrogenase (GDH) peaked at 50 days (senescent leaves). GDH deaminating activity increased 5-fold during the leaf development in HI plants, but only 2-fold in LI plants. The plants grown under HI exhibited considerable oxidative stress in vivo during the leaf senescence, as revealed by the substantial H2O2 accumulation and the sharply decrease in the antioxidant enzymes, catalase and ascorbate peroxidase, in comparison with LI plants. Probably, systemic signals triggered by a high PFD caused early senescence and diminished oxidative protection in primary leaves of sunflower plants as a result.

Additional key words: antioxidant enzymes; ascorbate peroxidase; catalase; glutamate dehydrogenase; glutamine synthetase; hexose; nitrite reductase; irradiance; nitrate reductase; plant; reactive oxygen species; senescence; sunflower; superoxide dismutase

Received: January 24, 2012; Accepted: October 24, 2012; Published: March 1, 2013  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
De La Mata, L., Cabello, P., De La Haba, P., & Agüera, E. (2013). Study of the senescence process in primary leaves of sunflower (Helianthus annuus L.) plants under two different light intensities. Photosynthetica51(1), 85-94. doi: 10.1007/s11099-013-0001-x
Download citation

References

  1. Adams, W.W., III, Zarter, C.R., Ebbert, V., Demmig-Adams, B.: Photoprotective strategies of overwintering evergreens. - BioScience 54: 41-49, 2004. Go to original source...
  2. Aebi, H.E.: Catalase. - In: Bergmeyer, H.U., Grassl, M. (ed.): Methods of Enzymatic Analysis. Pp. 273-286. Verlag Chemie, Weinheim 1983.
  3. Agüera, E., Poblete, L., de la Haba, P., Maldonado, J. M.: Light modulation and in vitro effects of adenine nucleotides on leaf nitrate reductase activity in cucumber (Cucumis sativus). - Physiol. Plant. 105: 218-223, 1999. Go to original source...
  4. Agüera, E., Ruano, D., Cabello, P., de la Haba, P.: Impact of atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in cucumber (Cucumis sativus L.) plants. - J. Plant Physiol. 163: 809-817, 2006. Go to original source...
  5. Agüera, E., Cabello, P., de la Haba, P.: Induction of leaf senescence by low nitrogen nutrition in sunflower (Helianthus annuus) plants. - Physiol. Plant. 138: 256-267, 2010. Go to original source...
  6. Ariz, I., Esteban, R., García-Plazaola, J.I., Becerril, J.M. et al.: High irradiance induces photoprotective mechanisms and a positive effect on NH4 + stress in Pisum sativum L. - J. Plant Physiol. 167: 1038-1045, 2010. Go to original source...
  7. Arzamendi, G., Campo, I., Arguiñarena, E., Sánchez, M., Montes, M., Gandía, L.M.: Synthesis of biodiesel from sunflower oil with silica-supported NaOH catalysts. - J. Chem. Technol. Biotechnol. 83: 862-870, 2008. Go to original source...
  8. Asada, K.: The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 601-639, 1999. Go to original source...
  9. Astolfi, S., De Biasi, M.G., Passera, C.: Effects of irradiance-sulphur interactions on enzymes of carbon, nitrogen and sulphur metabolism in maize plants. - Photosynthetica 39: 177-181, 2001. Go to original source...
  10. Baig, M.J., Anand, A., Mandal, P.K., Bhatt, R.K.: Irradiance influences contents of photosynthetic pigments and proteins in tropical grasses and legumes. - Photosynthetica 43: 47-53, 2005. Go to original source...
  11. Behera, R.K., Choudhury, N.K.: Photosynthetic characteristics of chloroplasts of primary wheat leaves grown under different irradiance. - Photosynthetica 39: 11-15, 2001. Go to original source...
  12. Behera, R.K., Choudhury, N.K.: High irradiance-induced changes in carotenoid composition and increase in nonphotochemical quenching of Chl a fluorescence in primary wheat leaves. - J. Plant Physiol. 160: 1141-1146, 2003. Go to original source...
  13. Beutler, H.O.: D-Fructose. - In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. Pp. 321-327. Verlag Chemie, Weinheim 1984.
  14. Bradford, M.M.: A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  15. Buchanan-Wollaston, V., Earl, E., 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, 2003a. Go to original source...
  16. Buchanan-Wollaston, V., Wellesbourne, H.R.I., Warwick, U.K.: Senescence, leaves. - In: Encyclopedia of Applied Plant Sciences, Elsevier Academic Press. Pp. 808-816, 2003b. Go to original source...
  17. Cabello, P., de la Haba, P., González-Fontes, A., Maldonado, J.M.: Induction of nitrate reductase, nitrite reductase, and glutamine synthetase isoforms in sunflower cotyledons as affected by nitrate, light, and plastid integrity. - Protoplasma 201: 1-7, 1998. Go to original source...
  18. Cabello, P., Agüera, E., de la Haba, P.: Metabolic changes during natural ageing in sunflower (Helianthus annuus) leaves: expression and activity of glutamine synthetase isoforms are regulated differently during senescence. - Physiol. Plant. 128: 175-185, 2006. Go to original source...
  19. Cantamutto, M., Poverene, M.: Genetically modified sunflower release: opportunities and risks. Field Crop. Res. 101: 133-144, 2007. Go to original source...
  20. Carelli, M.L.C., Fahl, J.I., Cochicho J.D.: Aspects of nitrogen metabolism in coffee plants. - Braz. J. Plant Physiol. 18: 9-21, 2006. Go to original source...
  21. Couée, I., Sulmon, C., Gouesbet, G., El Amrani, A.: Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. - J. Exp. Bot. 3: 449-459, 2006. Go to original source...
  22. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzè, D., Van Breusegem, F.: Dual action of the active oxygen species during plant stress responses. - Cell. Mol. Life Sci. 57: 779-795, 2000. Go to original source...
  23. de la Haba, P., Cabello, P., Maldonado, J.M.: Glutaminesynthetase isoforms appearing in sunflower cotyledons during germination. Effects of light and nitrate. - Planta 186: 577-581, 1992. Go to original source...
  24. de la Haba, P., Agüera, E., Benítez, L., Maldonado, J.M.: Modulation of nitrate reductase activity in cucumber (Cucumis sativus) roots. - Plant Sci. 161: 231-237, 2001. Go to original source...
  25. Demmig-Adams, B., Adams, W.W., III: Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. - New Phytol. 172: 11-21, 2006. Go to original source...
  26. Díaz, C., Purdy, S., Christ, A., Morot-Gaudry, J.F., Wingler, A., Masclaux-Daubresse, C.: Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach. - Plant Physiol. 138: 898-908, 2005. Go to original source...
  27. Díaz, C., Lemaître, T., Christ, A., et al.: Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. - Plant Physiol. 147: 1437-1449, 2008. Go to original source...
  28. Gan, S., Amasino, R.M.: Making sense of senescence. Molecular genetic regulation and manipulation of leaf senescence. - Plant Physiol. 113: 313-319, 1997. Go to original source...
  29. Guo, Y., Gan, S.: Leaf senescence: signals, execution, and regulation. - Curr. Top. Develop. Biol. 71: 83-112, 2005. Go to original source...
  30. Hernández, J.A., Escobar, C., Creissen, G., Mullineaux, P.M.: Role of hydrogen peroxide and the redox state of ascorbate in the induction of antioxidant enzymes in pea leaves under excess light stress. - Funct. Plant Biol. 31: 359-368, 2004. Go to original source...
  31. Hernández, J.A., Escobar, C., Creissen, G., Mullineaux, P.M.: Antioxidant enzyme in pea plants under high irradiance. - Biol. Plant. 50: 395-399, 2006. Go to original source...
  32. Hewitt, E.J.: Sand and water culture methods used in the study of plant nutrition. - Commonwealth Bureau of Horticultural and Plantation Crops, East Malling. Tech. Commun. No 22, 1966.
  33. Hörtensteiner, S., Feller, U.: Nitrogen metabolism and remobilization during senescence. - J. Exp. Bot. 53: 927-937, 2002. Go to original source...
  34. Kunst, A., Draeger, B., Ziegenhorn, J.: D-Glucose: UV-methods with hexokinase and glucose-6-phosphate dehydrogenase. - In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. Pp. 163-172. Verlag Chemie, Weinheim 1984.
  35. Lehmann, T., Ratajczak, L.: The pivotal role of glutamate dehydrogenase (GDH) in the mobilization of N and C from storage material to asparagine in germinating seeds of yellow lupine. - J. Plant Physiol. 165: 149-158, 2008. Go to original source...
  36. Lichtenthaler, H.K.: Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. - Photosynth. Res. 92: 163-179, 2007. Go to original source...
  37. Lim, P.O., Woo, H.R., Nam, H.G: Molecular genetics of leaf senescence in Arabidopsis. - Trends Plant Sci. 8: 272-278, 2003. Go to original source...
  38. Lim, P.O., Kim, H.J., Nam, H.G.: Leaf senescence. - Annu. Rev. Plant Biol. 58: 115-136, 2007. Go to original source...
  39. Logan, B.A. Kornyeyev, D., Hardison, J., Holaday, A.S.: The role of antioxidant enzymes in photoprotection. - Photosynth. Res. 88: 119-132, 2006. Go to original source...
  40. Loyola-Vargas, V.M., Sánchez de Jiménez, E.: Differential role of glutamate dehydrogenase in nitrogen metabolism of maize tissues. - Plant Physiol. 76: 536-540, 1984. Go to original source...
  41. Mani, D., Sharma, B., Kumar, C.: Phytoaccumulation, interaction, toxicity and remediation of cadmium from Helianthus annuus L. (sunflower). - Bull. Environ. Contam. Toxicol. 79: 71-79, 2007. Go to original source...
  42. Martínez, D.E., Costa, M.L., Guiamet, J.J.: Senescence-associated degradation of chloroplast proteins inside and outside the organelle. - Plant Biol. 10: 15-22, 2008. Go to original source...
  43. Masclaux, C., Valadier, M.H., Brugière, N., Morot-Gaudry, J.F., Hirel, B.: Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. - Planta 211: 510-518, 2000. Go to original source...
  44. Masclaux-Daubresse, C., Valadier, M.H., Carrayol, E., Reisdorf-Cren, M., Hirel, B.: Diurnal changes in the expression of glutamate dehydrogenase and nitrate reductase are involved in the C/N balance of tobacco source leaves. - Plant Cell Environ. 25: 1451-1462, 2002. Go to original source...
  45. Masclaux-Daubresse, C., Carrayol, E., Valadier, M.H.: The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites. - Planta 221: 580-588, 2005. Go to original source...
  46. Masclaux-Daubresse, C., Reisdorf-Cren, M., Pageau, K. et al.: Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. - Plant Physiol. 140: 444-456, 2006. Go to original source...
  47. Masclaux-Daubresse, C., Purdy, S., Lemaître, T., Pourtau, N., Taconnat, L., Renou, J. P., Wingler, A.: Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence. - Plant. Physiol. 143: 434-446, 2007. Go to original source...
  48. Melis, A.: Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? - Trends Plant Sci. 4: 130-135, 1999. Go to original source...
  49. Miflin, B.J., Lea, P.J.: Ammonium assimilation. - In: Miflin, B.J. (ed.): The Biochemistry of Plants Amino Acids and Derivatives. Pp. 169-202. Academic Press. New York-London - Toronto - Sydney - San Francisco 1980. Go to original source...
  50. Miflin, B.J., Habash, D.: The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. - J. Exp. Bot. 53: 979-987, 2002. Go to original source...
  51. Moore, B., Zhou, L., Rolland, F., et al.: Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. - Science 300: 332-336, 2003. Go to original source...
  52. Mukherjee, S.P., Choudhuri, M.A.: Implications of water stressinduced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. - Physiol. Plant. 58: 166-170, 1983. Go to original source...
  53. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
  54. Oliveira, I.C., Coruzzi, G.M.: Carbon and amino acids reciprocally modulate the expression of glutamine syntethase in Arabidopsis. - Plant Physiol. 121: 301-310, 1999. Go to original source...
  55. Ono, K., Nishi, Y., Watanabe, A., Terashima, I.: Possible mechanisms of adaptive leaf senescence. - Plant Biol. 3: 234-243, 2001. Go to original source...
  56. Ougham, H., Hörtensteiner, S., Armstead, I., Donnison, I., King, I., Thomas, H., Mur, L.: The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. - Plant Biol. 10: 4-14, 2008. Go to original source...
  57. Outlaw, W.H., Jr., Tarczynski, M.C.: Sucrose. - In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. Pp. 96-103. Verlag Chemie, Weinheim 1984.
  58. Pageau, K., Reisdorf-Cren, M., Morot-Gaudry, J.F., Masclaux-Daubresse, C.: The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. - J. Exp. Bot. 57: 547-557, 2006. Go to original source...
  59. Pahlich, E.: Remarks concerning the dispute related to the function of plant glutamate dehydrogenase: commentary. - Can. J. Bot. 74: 512-515, 1996. Go to original source...
  60. Parrott, D., Yang, L., Shama, L., Fischer, A.M.: Senecence is accelerated, and several proteases are induced by carbon "feast" conditions in barley (Hordeum vulgare L.) leaves. - Planta 222: 989-1000, 2005. Go to original source...
  61. Pompelli, M.F., Martins, S.C.V., Antunes, W.C., Chaves, A.R.M., DaMatta, F.M.: Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. - J. Plant Physiol. 167: 1052-1060, 2010. Go to original source...
  62. Pourtau, N., Jennings, R., Pelzer E. et al.: Effect of sugarinduced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. - Planta 224: 556-568, 2006. Go to original source...
  63. Prá¹il, O., Adir, N., Ohad, I.: Dynamic of PSII: Mechanism of photoinhibition and recovery process. - In: Baber, J. (ed.): The Photosystems: Structures, Function and Molecular Biology. Pp 295-348. Elsevier, Amsterdam - London - New York - Tokyo 1992. Go to original source...
  64. Procházková, D., Wilhelmová, N.: Leaf senescence and activities of the antioxidant enzymes. - Biol. Plant. 51: 401-406, 2007. Go to original source...
  65. Quirino, B.F., Noh, Y.S., Himelblau, E., Amasino, R.M.: Molecular aspects of leaf senescence. - Trends Plant Sci. 5: 278-282, 2000. Go to original source...
  66. Radochová, B., Tichá, I.: Excess irradiance causes early symptoms of senescence during leaf expansion in photoautotrophically in vitro grown tobacco plants. - Photosynthetica 46: 471-475, 2008. Go to original source...
  67. Schansker, G., van Rensen, J.J.S.: Performance of active Photosystem II centers in photoinhibited pea leaves. - Photosynth. Res. 62:175-184, 1999. Go to original source...
  68. ©pundová, M., Popelková, H., Ilík, P., et al.: Ultra-structural and functional changes in the chloroplasts of detached barley leaves senescing under dark and light conditions. - J. Plant Physiol. 160: 1051-1058, 2003. Go to original source...
  69. ©pundová, M., Slouková, K., Hunková, M., Nau¹, J.: Plant shading increases lipid peroxidation and intensifies senescence-induced changes in photosynthesis and activities of ascorbate peroxidase and glutathione reductase in wheat. - Photosynthetica 43: 403-409, 2005. Go to original source...
  70. Srivalli, B., Khanna-Chopra, R.: The developing reproductive 'sink' induces oxidative stress to mediate nitrogen mobilization during monocarpic senescence in wheat. - Biochem. Biophys. Res. Commun. 325: 198-202, 2004. Go to original source...
  71. Srivalli, B., Khanna-Chopra, R.: Delayed wheat flag leaf senescence due to removal of spikelets is associated with increased activities of leaf antioxidant enzymes, reduced glutathione/oxidized glutathione ratio and oxidative damage to mitochondrial proteins. - Plant Physiol. Biochem. 47: 663-670, 2009. Go to original source...
  72. Vanacker, H., Sandalio, L.M., Jiménez, A., et al.: Roles for redox regulation in leaf senescence of pea plants grown on different sources of nitrogen nutrition. - J. Exp. Bot. 57: 1735-1745, 2006. Go to original source...
  73. van Doorn, W.G.: Is the onset of senescence in leaf cells of intact plants due to low or high sugar level? - J. Exp. Bot. 59: 1963-1972, 2008. Go to original source...
  74. Wingler, A., Masclaux-Daubresse, C., Fischer, A.M.: Sugars, senescence and ageing in plants and heterotrophic organisms. - J. Exp. Bot. 60: 1063-1066, 2009. Go to original source...
  75. Wingler, A., Purdy, S., MacLean, J.A., Pourtau, N.: The role of sugars in integrating environmental signals during the regulation of leaf senescence. - J. Exp. Bot. 57: 391-399, 2006. Go to original source...
  76. Wingler, A., Roitsch, T.: Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. - Plant Biol. 10: 50-62, 2008. Go to original source...
  77. Yoo, S.D., Greer, D.H., Laing, W.A., McManus, M.T.: Changes in photosynthetic efficiency and carotenoid composition in leaves of white clover at different developmental stages. - Plant Physiol. Biochem. 41: 887-893, 2003. Go to original source...
  78. Yoshimura, K., Yabuta, Y., Ishikawa, T., Shigeoka, S.: Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. - Plant Physiol. 123: 223-234, 2000. Go to original source...
  79. Zimmermann, P., Zentgraf, U.: The correlation between oxidative stress and leaf senescence during plant development. - Cell. Mol. Biol. Lett. 10: 515-534, 2005.
  80. Zimmermann, P., Heinlein, C., Orendi, G., Zentgraf, U.: Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. - Plant Cell Environ. 29: 1049-1060, 2006. Go to original source...