Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves

Plant, Cell and Environment

Volumn 32, Issue 11, 2009, Pages 1538-1547

  Zhang, Ru ^a   Cruz, Jeffrey A ^b   Kramer, David M ^b   Magallanes Lundback, Maria E ^c   Dellapenna, Dean ^c   Sharkey, Thomas D ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

Author keywords

Chlorophyll a fluorescence; Electrochromic shift; Ion movement; Moderate heat stress; Proton conductance; QE; Transthylokoid proton motive force; Zeaxanthin

Indexed keywords

XANTHOPHYLL; ZEAXANTHIN;

ABSORPTION SPECTRUM; CAROTENOID; CHLOROPHYLL A; ENVIRONMENTAL STRESS; FLUORESCENCE; LEAF; PH; PHYTOCHEMISTRY; TEMPERATURE EFFECT; TOBACCO;

ARTICLE; HEAT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT; PH; PHOTOSYSTEM II; PHYSIOLOGY; PLANT LEAF; PROTON MOTIVE FORCE; RADIATION EXPOSURE; SPECTROSCOPY; THYLAKOID; TOBACCO;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; LIGHT; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; PROTON-MOTIVE FORCE; SPECTRUM ANALYSIS; THYLAKOIDS; TOBACCO; XANTHOPHYLLS;

NICOTIANA TABACUM;

EID: 70349855095     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2009.02018.x     Document Type: Article

References (54)

1. Avenson T.J., Cruz J.A. Kramer D.M. (2004) Modulation of energy dependent quenching of excitons (qE) in antenna of higher plants. Proceedings of the National Academy of Sciences of the United States of America 101, 5530 5535.
2. Avenson T.J., Kanazawa A., Cruz J.A., Takizawa K., Ettinger W.E. Kramer D.M. (2005) Integrating the proton circuit into photosynthesis: progress and challenges. Plant, Cell & Environment 28, 97 109.
3. Avenson T.J., Ahn T.K., Zigmantas D., Niyogi K.K., Li Z.R., Ballottari M., Bassi R. Fleming G.R. (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. Journal of Biological Chemistry 283, 3550 3558.
4. Baker N.R., Harbinson J. Kramer D.M. (2007) Determining the limitations and regulations of photosynthetic energy transduction in leaves. Plant, Cell & Environment 30, 107 125.
5. Berry J.A. Björkman O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491 543.
6. Bilger W., Björkman O. Thayer S.S. (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiology 91, 542 551.
7. Bukhov N.G., Wiese C., Neimanis S. Heber U. (1999) Heat sensitivity of chloroplasts and leaves: Leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynthesis Research 59, 81 93.
8. Bukhov N.G., Samson G. Carpentier R. (2000) Nonphotosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress. Steady-state rate. Photochemistry and Photobiology 72, 351 357.
9. Cruz J.A., Sacksteder C.A., Kanazawa A. Kramer D.M. (2001) Contribution of electric field δφ to steady-state transthylakoid proton motive force in vitro and in vivo. Control of pmf parsing into δφ and δpH by counterion fluxes. Biochemistry 40, 1226 1237.
10. Feller U., Crafts-Brandner S.J. Salvucci M.E. (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiology 116, 539 546.
11. Havaux M. (1996) Short-term responses of photosystem I to heat stress - induction of a PS II-independent electron transport through PS I fed by stromal components. Photosynthesis Research 47, 85 97.
12. Havaux M. (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3, 147 151.
13. Havaux M. Tardy F. (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198, 324 333.
14. Havaux M., Greppin H. Strasser R.J. (1991) Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186, 88 98.
15. Havaux M., Tardy F., Ravenel J., Chanu D. Parot P. (1996) 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 & Environment 19, 1359 1368.
16. Havaux M., Dall'Osto L. Bassi R. (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiology 145, 1506 1520.
17. Horton P., Ruban A.V., Rees D., Pascal A.A., Noctor G. Young A.J. (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the Lhcii chlorophyll protein complex. FEBS Letters 292, 1 4.
18. Horton P., Ruban A.V. Walters R.G. (1996) Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 655 684.
19. Horton P., Wentworth M. Ruban A. (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Letters 579, 4201 4206.
20. Junge W., Ausländer W., McGeer A.J. Runge T. (1979) The buffering capacity of the internal phase of thylakoids and the magnitude of the pH changes inside under flashing light. Biochimica et Biophysica Acta 546, 121 141.
21. Kanazawa A. Kramer D.M. (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proceedings of the National Academy of Sciences of the United States of America 99, 12789 12794.
22. Kobza J. Edwards G.E. (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69 74.
23. Kramer D.M. Sacksteder C.A. (1998) A diffused-optics flash kinetic spectrophotometer (DOFS) for measurements of absorbance changes in intact plants in the steady-state. Photosynthesis Research 56, 103 112.
24. Kramer D.M., Cruz J.A. Kanazawa A. (2003) Balancing the central roles of the thylakoid proton gradient. Trends in Plant Science 8, 27 32.
25. Li X.P., Bjorkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S. Niyogi K.K. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391 395.
26. Li X.P., Müller-Moulé P., Gilmore A.M. Niyogi K.K. (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the United States of America 99, 15222 15227.
27. Li X.P., Gilmore A.M., Caffarri S., Bassi R., Golan T., Kramer D. Niyogi K.K. (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. Journal of Biological Chemistry 279, 22866 22874.
28. Lim B.P., Nagao A., Terao J., Tanaka K., Suzuki T. Takama K. (1992) Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. Biochimica et Biophysica Acta 1126, 178 184.
29. Müller P., Li X.P. Niyogi K.K. (2001) Non-photochemichal quenching. A response to excess light energy. Plant Physiology 125, 1558 1566.
30. Niyogi K.K. (2000) Safety valves for photosynthesis. Current Opinions in Plant Biology 6, 455 460.
31. Pastenes C. Horton P. (1996) Effect of high temperature on photosynthesis in beans. 1. Oxygen evolution and chlorophyll fluorescence. Plant Physiology 112, 1245 1251. (Pubitemid 26420656)
32. Pfündel E.E. Dilley R.A. (1993) The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts. Plant Physiology 101, 65 71.
33. Sacksteder C.A., Kanazawa A., Jacoby M.E. Kramer D.M. (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton pumping Q cycle is continuously engaged. Proceedings of the National Academy of Sciences of the United States of America 97, 14283 14288.
34. Salvucci M.E. Crafts-Brandner S.J. (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120, 179 186.
35. Salvucci M.E., Osteryoung K.W., Crafts-Brandner S.J. Vierling E. (2001) Exceptional sensitivity of rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiology 127, 1053 1064.
36. Sarry J.E., Montillet J.L., Sauvaire Y. Havaux M. (1994) The protective function of the xanthophyll cycle in photosynthesis. FEBS Letters 353, 147 150.
37. Schrader S.M., Wise R.R., Wacholtz W.F., Ort D.R. Sharkey T.D. (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant, Cell & Environment 27, 725 735.
38. Schröppel-Meier G. Kaiser W.M. (1988) Ion homeostasis in chloroplasts under salinity and mineral deficiency. Plant Physiology 87, 822 827.
39. Sharkey T.D. (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant, Cell & Environment 28, 269 277.
40. Sharkey T.D. Schrader S.M. (2008) High temperature stress. In Physiology and Molecular Biology of Stress Tolerance in Plants eds K.V.M. Rao, A.S. Raghavendra K.J. Reddy pp. 101 130. Springer, Dordrecht, the Netherlands.
41. Takizawa K., Cruz J.A., Kanazawa A. Kramer D.M. (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochimica et Biophysica Acta 1767, 1233 1244.
42. 1 ATP synthase. Plant, Cell & Environment 31, 235 243.
43. Teardo E., Laureto P.P., Bergantino E., Vecchia F.D., Rigoni F., Szabò I. Giacometti G.M. (2007) Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochimica et Biophysica Acta 1767, 703 711.
44. + and Cl- activity in the green alga Eremosphaera viridis. Plant Physiology 99, 103 110.
45. Tian L. DellaPenna D. (2001) Characterization of a second carotenoid β-hydroxylase gene from Arabidopsis and its relationship to the LUT1 locus. Plant Molecular Biology 47, 379 388.
46. Tian L., Magallanes-Lundback M., Musetti V. DellaPenna D. (2003) Functional analysis of β- and η-ring carotenoid hydroxylases in Arabidopsis. The Plant Cell 15, 1320 1332.
47. Vredenberg W.J. Bulychev A.A. (1976) Changes in the electrical potential across the thylakoid membranes of illuminated intact chloroplasts in the presence of membrane-modifying agents. Plant Science Letters 7, 101 107.
48. Weis E. (1980) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151, 33 39.
49. Weis E. (1981) Reversible effects of high, sublethal temperatures on light-induced light scattering changes and electrochromic pigment absorption shift in spinach leaves. Zeitschrift fur Pflanzenphysiologie 101, 169 178.
50. Weis E. (1982) Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Plant Physiology 70, 1530 1534.
51. Wise R.R. Ort D.R. (1989) Photophosphorylation after chilling in the light: effects on membrane energization and coupling factor activity. Plant Physiology 90, 657 664.
52. Witt H.T. (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochimica et Biophysica Acta 505, 355 427.
53. Yamamoto H.Y. Bassi R. (1996) Carotenoids: localization and function. In Oxygenic Photosynthesis: The Light Reactions (eds D.R. Ort C.F. Yocum pp. 539 563. Springer, the Netherlands.
54. Zhang R. Sharkey T.D. (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynthesis Research 100, 29 43.