Effects of moderate heat stress on photosynthesis: Importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene

Plant, Cell and Environment

Volumn 28, Issue 3, 2005, Pages 269-277

  Sharkey, Thomas D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Heat stress; Isoprene; Photosynthesis; Reactive oxygen species; Rubisco; Thylakoid reactions

Indexed keywords

PHOTOSYNTHESIS; STRESS; TEMPERATURE;

EID: 14644404385     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2005.01324.x     Document Type: Review

References (96)

1. Affek H.P. & Yakir D. (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiology 129, 269-277.
2. Allen J.F. (1992) Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta 1098, 275-335.
3. Armond P.A., Björkman O. & Staehelin H.A. (1980) Disociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus. Biochimica et Biophysica Acta 601, 433-442.
4. Asada K. (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601-639.
5. Barua D., Downs C.A. & Heckathorn S.A. (2003) Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Functional Plant Biology 30, 1071-1079.
6. Bernacchi C.J., Pimentel C. & Long S.P. (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant, Cell and Environment 26, 1419-1430.
7. Bernacchi C.J., Singsaas E.L., Pimentel C., Portis A.R. Jr & Long S.P. (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell and Environment 24, 253-259.
8. Berry J.A. & Björkman O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491-543.
9. Boucher N., Harnois J. & Carpentier R. (1989) Heat-stress stimulation of electron flow in a photosystem I submembrane fraction. Biochemistry and Cell Biology 68, 999-1004.
10. Bukhov N.G. & Carpentier R. (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiologia Plantarum 110, 279-285.
11. Bukhov N.G., Boucher N. & Carpentier R. (1998) Loss of the precise control of photosynthesis and increased yield of non-radiative dissipation of excitation energy after mild heat treatment of barley leaves. Physiologia Plantarum 104, 563-570.
12. 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.
13. 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.
14. Carlberg I., Hansson M., Kieselbach T., Schröder W.P., Andersson B. & Vener A.V. (2003) A novel plant protein undergoing light-induced phosphorylation and release from the photosynthetic thylakoid membranes. Proceedings of the National Academy of Sciences of the USA 100, 757-762.
15. Chow W.S., Miller C. & Anderson J.M. (1991) Surface charges, the heterogeneous lateral distribution of the two photosystems, and thylakoid stacking. Biochimica et Biophysica Acta 1057, 69-77.
16. Çjánek M., Štroch M., Lachetová K., Kalina J. & Špunda V. (1998) Characterization of the photosystem II inactivation of heat-stressed barley leaves as monitored by the various parameters of chlorophyll a fluorescence and delayed fluorescence. Journal of Photochemistry and Photobiology 47, 39-45.
17. 2. Proceedings of the National Academy of Sciences of the USA 97, 13430-13435.
18. 6f complex. Biochemistry 43, 5921-5929.
19. Demmig-Adams B. & Adams W.W. III (1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599-626.
20. Depège N., Bellafiore S. & Rochaix J.D. (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299, 1572-1575.
21. Downs C.A., Coleman J.S. & Heckathorn S.A. (1999) The chloroplast 22-Ku heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. Journal of Plant Physiology 155, 477-487.
22. Egorova E.A. & Bukhov N.G. (2002) Effects of elevated temperatures on the activity of alternative pathways of photosynthetic electron transport in intact barley and maize leaves. Russian Journal of Plant Physiology (Abstract Only) 49, 575-584.
23. Enami I., Kitamura M., Tomo T., Isokawa Y., Ohta H. & Katoh S. (1994) Is the primary cause of thermal inactivation of oxygen evolution in spinach PSII membranes release of the extrinsic 33 kDa protein or Mn? Biochimica et Biophysica Acta 1186, 52-58.
24. 3 species. Planta 149, 78-90.
25. 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.
26. Furbank R.T. & Badger M.R. (1983) Oxygen exchange associated with electron transport and photophosphorylation in spinach thylakoids. Biochimica et Biophysica Acta 723, 400-409.
27. Gombos Z., Wada H., Hideg E. & Murata N. (1994) The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiology 104, 563-567.
28. Gounaris K., Brain A.P.R., Quinn P.J. & Williams W.P. (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochimica et Biophysica Acta 766, 198-208.
29. Haldimann P. & Feller U. (2004) 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 and Environment 27, 1169-1183.
30. Haldimann P. & Feller U. (2005) Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves. Plant, Cell and Environment 28, 00-00.
31. Hammer M.F., Markwell J. & Sarath G. (1997) Purification of a protein phosphatase from chloroplast stroma capable of dephosphorylating the light-harvesting complex-II. Plant Physiology 113, 227-233.
32. Hanson D.T., Swanson S., Graham L.E. & Sharkey T.D. (1999) Evolutionary significance of isoprene emission from mosses. American Journal of Botany 86, 634-639.
33. Hansson M. & Vener A.V. (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Molecular and Cellular Proteomics 2, 550-559.
34. Harrison M.A. & Allen J.F. (1991) Light-dependent phosphorylation of Photosystem II polypeptides maintains electron transport at high light intensity: Separation from effects of phosphorylation of LHC-II. Biochimica et Biophysica Acta 1058, 289-296.
35. 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.
36. Havaux M. & Gruszecki W.I. (1993) Heat- and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin: indications of a regulatory effect of zeaxanthin on membrane fluidity. Photochemistry and Photobiology 58, 607-617.
37. Havaux M. & Tardy F. (1996) Temperature-dependent adjustment of the thermal stability of Photosystem II in vivo: possible involvement of xanthophyl-cycle pigments. Planta 198, 324-333.
38. 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 and Environment 19, 1359-1368.
39. Heber U. (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynthesis Research 73, 223-231.
40. Heber U. & Walker D. (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiology 100, 1621-1626.
41. Heckathorn S.A., Downs C.A., Sharkey T.D. & Coleman J.S. (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology 116, 439-444.
42. Heckathorn S.A., Ryan S.L., Baylis J.A., Wang D.F., Hamilton E.W. III, Cundiff L. & Luthe D.S. (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Functional Plant Biology 29, 933-944.
43. Houghton J.T., Ding Y., Griggs D.J et al. (2001) Climate Change 2001: the Scientific Basis, pp. 1-881. Cambridge University Press, Cambridge, UK. (www.ipcc.ch)
44. IPCC (2001) Climate Change 2001: Impacts, Adaptation, and Vulnerability. Summary for Policy Makers. p. 50. IPCC, Geneva, Switzerland.
45. Joët T., Cournac L., Horvath E.M., Medgyesy P. & Peltier G. (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiology 125, 1919-1929.
46. 3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiology 128, 760-769.
47. Joliot P. & Joliot A. (2002) Cyclic electron transfer in plant leaf. Proceedings of the National Academy of Sciences of the USA 99, 10209-10214.
48. 2 production by Rubisco. FEBS Letters 571, 124-128.
49. Kobza J. & Edwards G.E. (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69-74.
50. Kühnemann F., Wolfertz M., Arnold A., Lagemann M., Popp A., Schüler G., Jux A. & Boland W. (2002) Simultaneous online detection of isoprene and isoprene-d2 using infrared photoacoustic spectroscopy. Applied Physical B 75, 397-403.
51. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 302, 1009-1014.
52. Law R. & Crafts-Brandner S.J. (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173-182.
53. Leakey A.D.B., Press M.C. & Scholes J.D. (2003) High-temperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling. Plant, Cell and Environment 26, 1681-1690.
54. Lobell D.B. & Asner G.P. (2003) Climate and management contributions to recent trends in U.S. agricultural yields. Science 299, 1032.
55. Logan B.A., Monson R.K. & Potosnak M.J. (2000) Biochemistry and physiology of foliar isoprene production. Trends in Plant Science 5, 477-481.
56. Loreto F. & Velikova V. (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology 127, 1781-1787.
57. Loreto F., Mannozzi M., Maris C., Nascetti P., Ferranti F. & Pasqualini S. (2001) Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiology 126, 993-1000.
58. Lu Z.M., Chen J.W., Percy R.G. & Zeiger E. (1997) Photosynthetic rate, stomatal conductance and leaf area in two cotton species (Gossypium barbadense and Gossypium hirsutum) and their relation with heat resistance and yield. Australian Journal of Plant Physiology 24, 693-700.
59. Lunde C., Jensen P.E., Haldrup A., Knoetzel J. & Scheller H.V. (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408, 613-615.
60. Makino A., Miyake C. & Yokota A. (2002) Physiological functions of the water-water cycle (Mehler Reaction) and the cyclic electron flow around PSI in rice leaves. Plant and Cell Physiology 43, 1017-1026.
61. Murakami Y., Tsuyama M., Kobayashi Y., Kodama H. & Iba K. (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287, 476-479.
62. 2 assimilation and metabolite contents. Plant Physiology 112, 1253-1260.
63. Peñuelas J., Llusià J., Asensio D. & Munné-Bosch S. (2005) Linking isoprene with plant thermotolerance, antioxidants, and monoterpene emissions. Plant, Cell and Environment 28, 00-00.
64. Perchorowicz J.T., Raynes D.A. & Jensen R.G. (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proceedings of the National Academy of Sciences of the USA 78, 2985-2989.
65. Pursiheimo S., Martinsuo P., Rintamaki E. & Aro E.M. (2003) Photosystem II protein phosphorylation follows four distinctly different regulatory patterns induced by environmental cues. Plant, Cell and Environment 26, 1995-2003.
66. Radin J.W., Lu Z., Percy R.G. & Zeiger E. (1994) Genetic variability for stomatal conductance in Pima cotton and its relation to improvements of heat adaptation. Proceedings of the National Academy of Sciences of the USA 91, 7217-7221.
67. Rokka A., Aro E.M., Herrmann R.G., Andersson B. & Vener A.V. (2000) Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiology 123, 1525-1535.
68. 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.
69. Santarius K.A. (1975) Sites of heat sensitivity in chloroplasts and differential inactivation of cyclic and noncyclic photophosphorylation by heating. Journal of Thermal Biology 1, 101-107.
70. Santarius K.A. & Müller M. (1979) Investigations on heat resistance of spinach leaves. Planta 146, 529-538.
71. 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 and Environment 27, 725-735.
72. Schreiber U., Heimann S. & Klughammer C. (1998) Two distinct states of the thylakoid bf complex. FEBS Letters 426, 126-130.
73. 4 intermediate photosynthesis in warm environments. Plant, Cell and Environment 13, 903-912.
74. 3 plants. Its occurrence and a possible explanation. Plant Physiology 78, 71-75.
75. 3 photosynthesis. Philosophical Transactions of the Royal Society of London B 323, 435-448.
76. Sharkey T.D. & Singsaas E.L. (1995) Why plants emit isoprene. Nature 374, 769.
77. Sharkey T.D., Badger M.R., Von Caemmerer S. & Andrews T.J. (2001a) Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynthesis Research 67, 147-156.
78. Sharkey T.D., Chen X.Y. & Yeh S. (2001b) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiology 125, 2001-2006.
79. Singsaas E.L., Laporte M.M., Shi J.-Z., Monson R.K., Bowling D.R., Johnson K., Lerdau M., Jasentuliyana A. & Sharkey T.D. (1999) Leaf temperature fluctuation affects isoprene emission from red oak (Quercus rubra) leaves. Tree Physiology 19, 917-924.
80. Singsaas E.L. & Sharkey T.D. (1998) The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant, Cell and Environment 21, 1181-1188.
81. Snyders S. & Kohorn B.D. (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. Journal of Biological Chemistry 274, 9137-9140.
82. Snyders S. & Kohorn B.D. (2001) Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. Journal of Biological Chemistry 276, 32169.
83. o chlorophyll fluorescence. Plant Physiology 91, 1494-1500.
84. Thomas P.G., Dominy P.J., Vigh L., Mansourian A.R., Quinn P.J. & Williams W.P. (1986) Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochimica et Biophysica Acta 849, 131-140.
85. Thompson L.K., Blaylock R., Sturtevant J.M. & Brudvig G.W. (1989) Molecular basis of the heat denaturation of photosystem II. Biochemistry 28, 6686-6695.
86. Velikova V. & Loreto F. (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from heat stress. Plant, Cell and Environment 28, 00-00.
87. Vener A.V., Harms A., Sussman M.R. & Vierstra R.D. (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. Journal of Biology Chemistry 276, 6959-6966.
88. Vener A.V., Rokka A., Fulgosi H., Andersson B. & Herrmann R.G. (1999) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38, 14955-14965.
89. Vener A.V., van Kan P.J.M., Gal A., Andersson B. & Ohad I. (1995) Activation/deactivation cycle of redox-controlled thylakoid protein phosphorylation. Journal of Biological Chemistry 270, 25225-25232.
90. Vijayan P. & Browse J. (2002) Photoinhibition in mutants of Arabidopsis deficient in thylakoid unsaturation. Plant Physiology 129, 876-885.
91. Weis E. (1980) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151, 33-39.
92. Wise R.R., Olson A.J., Schrader S.M. & Sharkey T.D. (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant, Cell and Environment 27, 717-724.
93. Wolfertz M., Sharkey T.D., Boland W. & Kühnemann F. (2004) Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis. Plant Physiology 135, 1939-1945.
94. Yamane Y., Kashino Y., Koike H. & Satoh K. (1998) Effects of high temperatures on the photosynthetic systems in spinach: Oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynthesis Research 57, 51-59.
95. o increases by high temperatures in higher plants. Photosynthesis Research 63, 23-34.
96. Zeidler J., Schwender J., Müller C., Wiesner J., Weidemeyer C., Beck E., Jomaa H. & Lichtenthaler H.K. (1998) Inhibition of the non-mevalonate 1-deoxy-D-xylulose-5-phosphate pathway of plant isoprenoid biosynthesis by fosmidomycin. Zeitschrift Fur Naturforschung C 53, 980-986.