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Photosynthetica

, 49:435 | Cite as

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

  • W. Xue
  • X. Y. Li
  • L. S. Lin
  • Y. J. Wang
  • L. Li
Original Papers

Abstract

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.

Additional key words

Alhagi sparsifoliaelevated temperature oxidative species photosystem II Rubisco activity 

Abbreviations

ABS/CSm

the specific energy fluxes (per cross section) for absorption

Cars

carotenoids

Chl

chlorophyll

Ci

the intercellular CO2 concentration

DIo/CSm

the dissipated energy flux per cross section

ETo/CSm

the electron transport flux per cross section

Fo

the minimal fluorescence of the dark adapted state

Fm

the maximal fluorescence of the dark adapted state

Fv/Fm

the maximum photochemical efficiency of PSII

H2O2

hydrogen peroxide

HO·

hydroxyl radical

OEC

oxygenevolving complexes

O2·−

superoxide

RA

Rubisco activase

RCs

the number of active reaction centers per cross section

Rp

the photorespiration rate

PI

leaf vitality index

PSII

photosystem II

ROS

reactive oxygen species

PN

the rate of CO2 assimilation

TRo/CSm

the trapped energy fluxes per cross section

Notes

Acknowledgments

This research was supported by the National Basic Research Program of China (2009CB421303), the key program for Science and Technology Development of Xinjiang (200933125), and the key Project in the National Science and Technology Pillar Program (2009BAC54B03). We thank anonymous reviewers for their valuable comments on the version of the manuscript.

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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.]Google Scholar
  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.]Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  18. Hideg, É., Vass, I.: The 75 °C thermoluminescence band of green tissues: chemiluminescence from membrane-chlorophyll interaction. — Photochem. Photobiol. 58: 280–283, 1993.CrossRefGoogle Scholar
  19. Horemans, N., Foyer, C., Potters, G., Asard, H.: Ascorbate function and associated transport systems in plants. — Plant Physiol. Biochem. 38: 531–540, 2000.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  24. Krause, G.H., Weis, E.: Chlorophyll fluorescence as a tool in plant. II. Interpretation of fluorescence signals. — Photosynth. Res. 5: 139–157, 1984.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  29. Li, H.S.: [Technology of Plant physiological biochemical experiment.] — China Higher Education Press, Beijing 2000. [In Chin.]Google Scholar
  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.Google Scholar
  31. Lichtenthaler, H.K.: The stress concept in plants: an introduction. — Ann. N.Y. Acad. Sci. 851: 187–198, 1998.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  33. Lu, C.M., Zhang, J.H.: Heat-induced multiple effects on PSII in wheat plants. — J. Plant Physiol. 156: 259–265, 2000.Google Scholar
  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.]Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.]Google Scholar
  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.PubMedCrossRefGoogle Scholar
  47. Somersalo, S., Krause, G.H.: Photoinhibition at chilling temperature: fluorescence characterisitics of unhardened and cold-acclimated spinach leaves. — Planta 177: 409–416, 1989.CrossRefGoogle Scholar
  48. Srivastava, A., Strasser, R.J.: Stress and stress management of land plants during a regular day. — J. Plant Physiol. 148: 445–455, 1996.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  51. Strasser, B.J.: Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. — Photosynth. Res. 52: 147–155, 1997.CrossRefGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  54. Triantaphylidès, C., Havaux, M.: Singlet oxygen in plants: production, detoxification and signaling. — Trends Plant Sci. 14: 219–228, 2009.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  58. Xu, D.Q., Shen, Y.G.: [Plant Physiolog and Molecular Biology: The restrained factors of photosynthesis.] —Science Press, Beijing 1998. [In Chin.]Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  62. Yamashita, T., Butler, W.: Inhibition of chloroplasts by UV-irradiation and heat-treatment. — Plant Physiol. 43: 2037–2040, 1968.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • W. Xue
    • 1
    • 2
    • 3
  • X. Y. Li
    • 2
    • 3
  • L. S. Lin
    • 1
    • 3
  • Y. J. Wang
    • 1
    • 2
    • 3
  • L. Li
    • 1
    • 2
    • 3
  1. 1.Xinjiang Institute of Ecology and Geography, State Key Laboratory of Desert and Oasis EcologyChinese Academy of SciencesUrumqiChina
  2. 2.Graduate University of Chinese Academy of SciencesBeijingChina
  3. 3.Cele National Station of Observation & Research for Desert Grassland EcosystemCeleXinjiang, China

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