Photosynthetica, 2011 (vol. 49), issue 3

Photosynthetica 2011, 49(3):435 | DOI: 10.1007/s11099-011-0054-7

Effects of elevated temperature on photosynthesis in desert plant Alhagi sparsifolia S

W. Xue1,2,3, X. Y. Li2,3,*, L. S. Lin1,3, Y. J. Wang1,2,3, L. Li1,2,3
1 Xinjiang Institute of Ecology and Geography, State Key Laboratory of Desert and Oasis Ecology, Chinese Academy of Sciences, Urumqi, China
2 Graduate University of Chinese Academy of Sciences, Beijing, China
3 Cele National Station of Observation & Research for Desert Grassland Ecosystem, Cele, Xinjiang, China

Most plants growing in temperate desert zone exhibit brief temperature-induced inhibition of photosynthesis at midday in the summer. Heat stress has been suggested to restrain the photosynthesis of desert plants like Alhagi sparsifolia S. It is therefore possible that high midday temperatures damage photosynthetic tissues, leading to the observed inhibition of photosynthesis. In this study, we investigated the mechanisms underlying heat-induced inhibition of photosynthesis in A. sparsifolia, a dominant species found at the transition zone between oasis and sandy desert on the southern fringe of the Taklamakan desert. The chlorophyll (Chl) a fluorescence induction kinetics and CO2 response curves were used to analyze the thermodynamic characters of both photosystem II (PSII) and Rubisco after leaves were exposed to heat stress. When the leaves were heated to temperatures below 43°C, the initial fluorescence of the dark-adapted state (Fo), and the maximum photochemical efficiency of PSII (Fv/Fm), the number of active reaction centers per cross section (RCs) and the leaf vitality index (PI) increased or declined moderately. These responses were reversed, however, upon cooling. Moreover, the energy allocation in PSII remained stable. The gradual appearance of a K point in the fluorescence curve at 48°C indicated that higher temperatures strongly impaired PSII and caused irreversible damage. As the leaf temperature increased, the activity of Rubisco first increased to a maximum at 34°C and then decreased as the temperature rose higher. Under high-temperature stress, cell began to accumulate oxidative species, including ammoniacal nitrogen, hydrogen peroxide (H2O2), and superoxide (O2 .-), suggesting that disruption of photosynthesis may result from oxidative damage to photosynthetic proteins and thylakoid membranes. Under heat stress, the biosynthesis of nonenzyme radical scavenging carotenoids (Cars) increased. We suggest that although elevated temperature affects the heat-sensitive components comprising of PSII and Rubisco, under moderately high temperature the decrease in photosynthesis is mostly due to inactivation of dark reactions.

Keywords: Alhagi sparsifolia S; elevated temperature; oxidative species; photosystem II; Rubisco activity

Received: November 9, 2010; Accepted: July 4, 2011; Published: September 1, 2011Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Xue, W., Li, X.Y., Lin, L.S., Wang, Y.J., & Li, L. (2011). Effects of elevated temperature on photosynthesis in desert plant Alhagi sparsifolia S. Photosynthetica49(3), 435. doi: 10.1007/s11099-011-0054-7.
Download citation

References

  1. Appenroth, K.J., Stöckel, J., Srivastava, A., Strasser, R.J.: Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. - Environ. Pollut. 115: 49-64, 2001. Go to original source...
  2. Bloom, A.J.: Nitrogen as a limiting factor: crop acquisition of ammonium and nitrate. - In: Jackson, L.E. (ed.): Ecology in Agriculture. Pp. 145-172. Academic Press, San Diego 1997. Go to original source...
  3. Bartošková, H., Komenda, J., Nauš, J.: Functional changes of photosystem II in the moss Rhizomnium punctatum (Hedw.) induced by different rates of dark desiccation. - J. Plant Physiol. 154: 597-604, 1999. Go to original source...
  4. Blokhina, O., Fagerstedt, K.V.: Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. - Physiol. Plant. 138: 447-462, 2010. Go to original source...
  5. Bruelheide, H., Vonlanthen, B., Jandt, U., Thomas, F..M., Foetzki, A., Gries, D., Wang, G., Zhang, X.M., Runge, M.: Life on the edge - to which degree does phreatic water sustain vegetation in the periphery of the Taklamakan Desert? - Appl. Veg. Sci. 13: 56-71, 2010. Go to original source...
  6. Bukhov, N.G., Carpentier, R.: Heterogeneity of photosystem II reaction centersas influenced by heat treatment of barley leves. - Physiol. Plant. 110: 279-285, 2000. Go to original source...
  7. Bukhov, N.G., Mohanty, P.: Elevated temperature stress effects on photosystems:characterization and evaluation of the nature of heat induced impairments. - In: Singhal, G.S., Renger, G., Sopory, S.K., Irrgang, K.D., Govingjee (ed.): Concepts in Photobiology: Photosynthesis and Photomorphogenesis. Pp. 617-648. Narosa Publ. House, New Delhi 1999. Go to original source...
  8. Costa, E.S., Bressan-Smith, R., Oliveira, J.G., Campostrini, E., Pimentel, C.: Photochemical efficiency in bean plants during recovery from high temperature stress. - Braz. J. Plant Physiol. 14: 105-110, 2002. Go to original source...
  9. Crafts-Brandner, S.J., Salvucci, M.E.: Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. - Proc. Natl. Acad. Sci. USA 97: 13430-13435, 2000. Go to original source...
  10. Deng, X., Li, X.M., Zhang, X.M., Ye, W.H., Zhao, Q.: [Relationship between gas exchange of four desert plants and environmental factors in Taklimakan.] - Chin. J. Appl. Environ. Biol. 8: 445-452, 2002. [In Chin.]
  11. [Experimental Guide of Modern Plant Physiology. - In: Shanghai Institute of Plant Physiology, The Shanghai Society for Plant Physiology (edu.): Physiological resistance.] Pp. 138-308, Science Press, Beijing 2004. [In Chin.]
  12. Ferguson, I.B., Watkins, C.B., Harman, J.E.: Inhibition by calcium of senescence of detached cucumber cotyledons: effect on ethylene and hydroperoxide production. - Plant Physiol. 71: 182-186, 1983. Go to original source...
  13. Goltsev, V., Yordanov, I., Tsonev, T.: Evaluation of relative contribution of initial and variable chlorophyll fluorescence measured at different temperatures. - Photosynthetica 30: 629-643, 1994.
  14. Guissé, B., Srivastava, A., Strasser, R.J.: The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves. - Arch. Sci. 48: 147-160, 1995.
  15. Havaux, M., Tardy, F., Ravenel, J., Chanu, D., Parot, P.: Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. - Plant Cell Environ. 19: 1359-1368, 1996. Go to original source...
  16. Haldimann, P., Feller, U.: Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose 1,5-bisphosphate carboxylase/oxygenase. - Plant Cell Environ. 27: 1169-1183, 2004. Go to original source...
  17. Haldimann, P., Strasser, R.J.: Effects of anaerobiosis as probed by the polyphasic Chl a fluorescence rise kinetics in pea. - Photosynth. Res. 62: 67-83, 1999. Go to original source...
  18. Hideg, É., Vass, I.: The 75 °C thermoluminescence band of green tissues: chemiluminescence from membrane-chlorophyll interaction. - Photochem. Photobiol. 58: 280-283, 1993. Go to original source...
  19. Horemans, N., Foyer, C., Potters, G., Asard, H.: Ascorbate function and associated transport systems in plants. - Plant Physiol. Biochem. 38: 531-540, 2000. Go to original source...
  20. IPCC.: Climate Change: Impacts, adaptation and vulnerability contribution of working group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. - Cambridge University Press, Cambridge - London - New York 2007.
  21. Kaňa, R., Kotabová, E., Prášil, O.: Acceleration of plastoquinone pool reduction by alternative pathways precedes a decrease in photosynthetic CO2 assimilation in preheated barley leaves. - Physiol. Plant. 133: 794-806, 2008. Go to original source...
  22. Kaňa, R., Vass, I.: Thermoimaging as a tool for studying lightinduced heating of leaves: correlation of heat dissipation with the efficiency of photosystem II photochemistry and nonphotochemical quenching. - Environ. Exp. Bot. 64: 90-96, 2008. Go to original source...
  23. Kubien, D.S., Sage, R.F.: The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. - Plant Cell Environ. 31: 407-418, 2008. Go to original source...
  24. Krause, G.H., Weis, E.: Chlorophyll fluorescence as a tool in plant. II. Interpretation of fluorescence signals. - Photosynth. Res. 5: 139-157, 1984. Go to original source...
  25. Lambers, H., Chapin, F.S. III, Pons, T.L.: Plant Physiological Ecology. - In: Clarkson, D.T. (ed.): Photosynthesis. Pp. 8-68. Springer-Verlag, Berlin - Heidelberg 1998. Go to original source...
  26. Lazár, D.: Modelling of light-induced chlorophyll a fluorescence rise (OJIP transient) and changes in 820 nmtransmittance signal of photosynthesis. - Photosynthetica 47: 483-498, 2009. Go to original source...
  27. Lazár, D., Ilík, P., Kruk, J., Strzałka, K., Nauš, J.: A theoretical study on effect of the initial redox state of cytochrome b559 on maximal chlorophyll fluorescence level (FM): implications for photoinhibition of photosystem II. - J. Theor. Biol. 233: 287-300, 2005. Go to original source...
  28. Lee, S.H., Ahsan, N., Lee, K.W., Kim, D.H., Lee, D.G., Kwak, S.S., Kwon, S.Y., Kim, T.H., Lee, B.H.: Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. - J. Plant Physiol. 164: 1626-1638, 2007. Go to original source...
  29. Li, H.S.: [Technology of Plant physiological biochemical experiment.] - China Higher Education Press, Beijing 2000. [In Chin.]
  30. Li, X.Y., Zhang, X.M., Zeng, F.J., Foetzki, A., Thomas, F.M., Li, X.M., Runge, M., He, X.Y.: Water relations on Alhagi sparsifolia in the southern fringe of Taklamakan Desert. - Acta Bot. Sin. 44: 1219-1224, 2002.
  31. Lichtenthaler, H.K.: The stress concept in plants: an introduction. - Ann. N.Y. Acad. Sci. 851: 187-198, 1998. Go to original source...
  32. Lípová, L., Krchňák, P., Komenda, J., Ilík, P.: Heat-induced disassembly and degradation of chlorophyll-containing protein complexes in vivo. - Biochim. Biophys. Acta 1797: 63-70, 2010. Go to original source...
  33. Lu, C.M., Zhang, J.H.: Heat-induced multiple effects on PSII in wheat plants. - J. Plant Physiol. 156: 259-265, 2000. Go to original source...
  34. Lu, F.H., Ye, X.H., Yu, H.F., Dong, M.: [Clonal integration modifies responses of hedysarum laeve to local sand burial in Mu Us sandland.] - Chin. J. Plant Ecol. 30: 278-285, 2006. [In Chin.]
  35. Mathur, S., Jajoo, A., Mehta, P., Bharti, S.: Analysis of elevated temperature-induced inhibition of photosystem II by using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum astivum). - Plant Biol. 13: 1-6, 2011. Go to original source...
  36. Musil, C.F., van Heerden, P.D.R., Cilliers, C.D., Schmiedel, U.: Mild experimental climate warming induces metabolic impairment and massive mortalities in southern African quartz field succulents. - Environ. Exp. Bot. 66: 79-87, 2009. Go to original source...
  37. op den Camp, R.G.L., Przybyla, D., Ochsenbein, C., et al.: Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. - Plant Cell 15: 2320-2332, 2003.
  38. Oukarroum, A., Madidi, S.E., Schansker, G., Strasser, R.J.: Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. - Environ. Exp. Bot. 60: 438-446, 2007. Go to original source...
  39. Pospíšil, P., Dau, H.: Chlorophyll fluorescence transients of photosystem II membrane particles as a tool for studying photosynthetic coxygen evolution. - Photosynth. Res. 65: 41-52, 2000. Go to original source...
  40. Pospíšil, P., Šnyrychová, I., Nauš, J.: Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature: EPR spin-trapping study. - Biochim. Biophys. Acta 1767: 854-859, 2007.
  41. Robinson, S.P., Portis, A.R.: Involvement of stromal ATP in the light activation of ribulose 1, 5-bisphosphate carboxylase/oxygenase in intact chloroplasts. - Plant Physiol. 86: 293-298, 1988. Go to original source...
  42. Sage, R.F.: Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. - J. Exp. Bot. 53: 609-620, 2002. Go to original source...
  43. Salvucci, M.E., Crafts-Brandner, S.J.: Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. - Plant Physiol. 134: 1460-1470, 2004. Go to original source...
  44. Sharkey, T.D.: Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. - Plant Cell Environ. 28: 269-277, 2005. Go to original source...
  45. Shi, Y.F., Shen, Y.P.: [Signal, impact and outlook of climatic shift from warm-dry to warm-humid in Northwest China.] - Sci. Technol. Rev. 20: 54-57, 2003. [In Chin.]
  46. Snider, J.L., Oosterhuis, D.M., Kawakami, E.M.: Genotypic differences in thermotolerance are dependent upon prestress capacity for antioxidant protection of the photosynthetic apparatus in Gossypium hirsutum. - Physiol. Plant. 138: 268-277, 2010. Go to original source...
  47. Somersalo, S., Krause, G.H.: Photoinhibition at chilling temperature: fluorescence characterisitics of unhardened and cold-acclimated spinach leaves. - Planta 177: 409-416, 1989. Go to original source...
  48. Srivastava, A., Strasser, R.J.: Stress and stress management of land plants during a regular day. - J. Plant Physiol. 148: 445-455, 1996. Go to original source...
  49. Srivastava, A., Guissé, B., Greppin, H., Strasser, R.J.: Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. - Biochim. Biophys. Acta 1320: 95-106, 1997. Go to original source...
  50. Stasik, O., Jones, H.G.: Response of photosynthetic apparatus to moderate high temperature in contrasting wheat cultivars at different oxygen concentrations. - J. Exp. Bot. 58: 2133-2143, 2007. Go to original source...
  51. Strasser, B.J.: Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. - Photosynth. Res. 52: 147-155, 1997. Go to original source...
  52. Strasser, B.J., Strasser, R.J.: Measuring fast fluorescence transients to address environmental quetions: The JIP test. - In: Mathis, P. (ed.): Photosynthesis: from light to biosphere. Pp. 977-980. Kluwer Academic Publ., Dordrecht - Boston - London 1995. Go to original source...
  53. Strasser, R.J., Tsimilli-Michael, M., Srivastava, A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou, G.C., Govindjee (ed.): Chlorophyll a fluorescence: a signature of photosynthesis. Pp. 321-362. Springer-Verlag, Berlin 2004. Go to original source...
  54. Triantaphylidès, C., Havaux, M.: Singlet oxygen in plants: production, detoxification and signaling. - Trends Plant Sci. 14: 219-228, 2009. Go to original source...
  55. van Heerden, P.D.R., Strasser, R.J., Krüger, G.H.J.: Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics. - Physiol. Plant. 121: 239-249, 2004. Go to original source...
  56. Veres, S., Tóth, V.R., Láposi, R., Oláh, V., Lakatos, G., Mészáros, I.: Carotenoid composition and photochemical activity of four sandy grassland species. - Photosynthetica 44: 255-261, 2006. Go to original source...
  57. von Caemmerer, S., Evans, J.R., Hudson, G.S., Andrews, T.J.: The kinetics of ribulose-l, 5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. - Planta 195: 88-97, 1994. Go to original source...
  58. Xu, D.Q., Shen, Y.G.: [Plant Physiolog and Molecular Biology: The restrained factors of photosynthesis.] -Science Press, Beijing 1998. [In Chin.]
  59. Yamada, M., Hidaka, T., Fukamachi, H.: Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. - Sci. Hortic. 67: 39-48, 1996. Go to original source...
  60. Yamamoto, Y., Aminaka, R., Yoshioka, M., Khatoon, M., Komayama, K., Takenaka, D., Yamashita, A., Nijo, N., Inagawa, K., Morita, N., Sasaki, T., Yamamoto, Y.: Quality control of photosystem II: impact of light and heat stresses. - Photosynth Res. 98: 589-608, 2008. Go to original source...
  61. Yamane, Y., Kashino, Y., Koike, H., Satoh, K.: Increases in the fluorescence Fo level and reversible inhibition of photosystem II reaction center by high-temperature treatments in higher plants. - Photosynth Res. 52: 57-64, 1997. Go to original source...
  62. Yamashita, T., Butler, W.: Inhibition of chloroplasts by UV-irradiation and heat-treatment. - Plant Physiol. 43: 2037-2040, 1968. Go to original source...
  63. Yin, Y., Li, S.M., Liao, W.Q., Lu, Q.T., Wen, X.G., Lu, C.M.: Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. - J. Plant Physiol. 167: 959-966, 2010. Go to original source...
  64. Zeng, J., Zeng, F.J., Arndt, S.K., Guo, H.F., Yan, H.L., Xing, W.J., Liu, B.: Growth, physiological characteristics and ion distribution of NaCl stressed Alhagi sparsifolia seedlings. - Chin. Sci. Bull. 53: 169-176, 2008. Go to original source...
  65. Zhang, L., Xu, H., Yang, J.C., Li, W.D., Jiang, G.M., Li, Y.G.: Photosynthetic characteristics of diploid honeysuckle (Lonicera japonica Thunb.) and its autotetraploid cultivar subjected to elevated ozone exposure. - Photosynthetica 48: 87-95, 2010. Go to original source...
  66. Zhou, H.H., Chen, Y.N., Li, W.H., Chen, Y.P.: Photosynthesis of Populus euphratica in relation to groundwater depths and high temperature in arid environment, northwest China. - Photosynthetica 48: 257-268, 2010. Go to original source...
  67. Zhu, B.Q., Yang, X.P.: The ion chemistry of surface and ground waters in the Taklimakan Desert of Tarim Basin, Western China. - Chin. Sci. Bull. 52: 2123-2129, 2007. Go to original source...