When it is too hot for photosynthesis: Heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation

Plant, Cell and Environment

Volumn 34, Issue 1, 2011, Pages 113-126

  Hüve, Katja ^a   Bichele, Irina ^b   Rasulov, Bahtijor ^b   Niinemets, Ülo ^a  

^a ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

Cellular damage; Dynamic temperature environment; Heat stress; Phaseolus vulgaris; Photosynthetic electron transport; Respiration; Stress response

Indexed keywords

CHLOROPHYLL; HYDROGEN PEROXIDE;

CELL ORGANELLE; CHLOROPHYLL; ELECTRON; ENVIRONMENTAL STRESS; FLUORESCENCE; HEAT FLUX; INHIBITION; LEGUME; LOW TEMPERATURE; PERMEABILITY; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; REACTION KINETICS; THRESHOLD; TIME DEPENDENT BEHAVIOR;

ARTICLE; BEAN; CELL MEMBRANE PERMEABILITY; CELL RESPIRATION; CONVALESCENCE; CYTOLOGY; EVAPOTRANSPIRATION; FLUORESCENCE; HEAT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; TIME;

CELL MEMBRANE PERMEABILITY; CELL RESPIRATION; CHLOROPHYLL; FLUORESCENCE; HOT TEMPERATURE; HYDROGEN PEROXIDE; PHASEOLUS; PHOTOSYNTHESIS; PLANT LEAVES; PLANT TRANSPIRATION; RECOVERY OF FUNCTION; STRESS, PHYSIOLOGICAL; TIME FACTORS;

PHASEOLUS VULGARIS;

EID: 78649981528     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02229.x     Document Type: Article

References (73)

1. Allan A.A., Maddumage R., Simons J.L., Neill S.O. & Ferguson I.B. (2006) Heat-induced oxidative activity protects suspension-cultured plant cells from low temperature damage. Functional Plant Biology 33, 67-76.
2. Armond P.A., Schreiber U. & Björkman O. (1978) Photosynthetic acclimation to temperature in the desert shrub, Larrea divaricata. II. Light-harvesting efficiency and electron transport. Plant Physiology 61, 411-415.
3. Atkin O.K. & Tjoelker M.G. (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343-351.
4. Atkin O.K., Holly C. & Ball M.C. (2000) Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant, Cell & Environment 23, 15-26.
5. Atkin O.K., Zhang Q. & Wiskich J.T. (2002) Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox poise of the quinone pool. Plant Physiology 128, 212-222.
6. Atkin O.K., Bruhn D., Hurry V.M. & Tjoelker M. (2005) The hot and the cold: unraveling the variable response of plant respiration to temperature. Evans review no. 2. Functional Plant Biology 32, 87-105.
7. Berry J. & Björkman O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Reviews of Plant Physiology 31, 491-543.
8. Bilger H.W., Schreiber U. & Lange O.L. (1984) Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods. Oecologia 63, 256-262.
9. 0: a time-resolved analysis. Photosynthesis Research 48, 189-196.
10. Bukhov N.G. & Carpentier R. (2003) Measurement of photochemical quenching of absorbed quanta in photosystem I of intact leaves using simultaneous measurements of absorbance changes at 830 nm and thermal dissipation. Planta 216, 630-638.
11. 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.
12. Chen H.-M., Zhou J. & Dai Y.-R. (2000) Cleavage of lamin-like proteins in vivo and in vitro apoptosis of tobacco protoplasts induced by heat shock. FEBS Letters 480, 165-168.
13. Chou M., Chen Y.M. & Lin C.Y. (1989) Thermotolerance of isolated mitochondria associated with heat shock proteins. Plant Physiology 89, 617-621.
14. Covey-Crump E.M., Attwood R.G. & Atkin O.K. (2002) Regulation of root respiration in two species of Plantago that differ in relative growth rate: the effect of short- and long-term changes in temperature. Plant, Cell & Environment 25, 1501-1513.
15. 2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiology 116, 1351-1357.
16. Enami I., Kimura 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 of Mn? Biochimica et Biophysica Acta 1186, 52-58.
17. Gounaris K., Brain A.P.R., Quinn P.J. & Williams W.P. (1984) Structural re-organization of chloroplast thylakoid membranes in response to heat-stress. Biochimica et Biophysica Acta 766, 198-208.
18. 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 & Environment 27, 1169-1183.
19. Hamerlynck E.P. & Knapp A.K. (1994) Leaf-level responses to light and temperature in two co-occurring Quercus (Fagaceae) species: implications for tree distribution patterns. Forest Ecology and Management 68, 149-159.
20. 3 leaves to environmental factors. In Modeling Crop Photosynthesis - from Biochemistry to Canopy (ed. K.J. Boote), pp. 17-39. Agronomy and Crop Science Society of America, Madison, NJ.
21. Havaux M. (1992) Stress tolerance of Photosystem II in vivo. Antagonistic effects of water, heat and photoinhibition stress. Plant Physiology 100, 424-432.
22. Havaux M. (1993a) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Science 94, 19-33.
23. Havaux M. (1993b) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant, Cell & Environment 16, 461-467.
24. Havaux M. (1994) Temperature-dependent modulation of the photoinhibition-sensitivity of photosystem II in Solanum tuberosum leaves. Plant and Cell Physiology 35, 757-766.
25. Havaux M. (1996) Short-term responses of Photosystem I to heat stress. Induction of a PSII-independent electron transport through PS I fed by stromal components. Photosynthesis Research 47, 85-97.
26. 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.
27. Huber S.C. (1990) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiology 91, 656-662.
28. Huber S.C., Kerr P.S. & Rufty T.W. (1985) Diurnal changes in sucrose phosphate synthase activity in leaves. Physiologia Plantarum 64, 81-87.
29. Hüve K., Bichele I., Tobias M. & Niinemets Ü. (2006) Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential. Plant, Cell & Environment 29, 212-228.
30. June T., Evans J.R. & Farquhar G.D. (2004) A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. Functional Plant Biology 31, 275-283.
31. Kim K. & Portis A.R. Jr (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. Plant and Cell Physiology 46, 522-530.
32. King A.W., Gunderson C.A., Post W.M., Weston D.J. & Wullschleger S.D. (2006) Plant respiration in a warmer world. Science 312, 536-537.
33. Kubien D.S. & Sage R.F. (2008) The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. Plant, Cell & Environment 31, 407-418.
34. Laisk A., Rasulov B.H. & Loreto F. (1998) Thermoinhibition of photosynthesis as analyzed by gas exchange and chlorophyll fluorescence. Russian Journal of Plant Physiology 45, 412-421.
35. Laisk A., Oja V., Rasulov B., Rämma H., Eichelmann H., Kasparova I., Pettai H., Padu E. & Vapaavuori E. (2002) A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves. Plant, Cell & Environment 25, 923-943.
36. Larkindale J. & Knight M.R. (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128, 682-695.
37. Larkindale J., Hall J.D., Knight M.R. & Vierling E. (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiology 138, 882-897.
38. Leuning R. (2002) Temperature dependence of two parameters in a photosynthesis model. Plant, Cell & Environment 25, 1205-1210.
39. Levine A., Pennell R.I., Alvarez M.E., Palmer R. & Lamb C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology 6, 427-437.
40. McCabe P.F., Levine A., Meijer P.-J., Tapon N.A., Pennell R.I. & Leaver C.J. (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. The Plant Journal 12, 267-280.
41. Medlyn B.E., Dreyer E., Ellsworth D., et al. (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25, 1167-1179.
42. Nash D., Miyao M. & Murata N. (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochimica et Biophysica Acta 807, 127-133.
43. Niinemets Ü., Oja V. & Kull O. (1999) Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees. Plant, Cell & Environment 22, 1497-1514.
44. Ogawa T., Pan L., Kawai-Yamada M., Yu L.-H., Yamamura S., Koyama T., Kitajima S., Ohme-Takagi M., Sato F. & Uchimiya H. (2005) Functional analysis of Arabidopsis ethylene-responsive element binding protein conferring resistance to Bax and abiotic stress-induced plant cell death. Plant Physiology 138, 1436-1445.
45. De Pinto M.C., Paradiso A., Leonetti P. & De Gara L. (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. The Plant Journal 48, 784-795.
46. Raghavendra A.S. & Padmasree K. (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8, 546-553.
47. Ribeiro R.V., Machado E.C. & De Oliveira R.F. (2006) Temperature response of photosynthesis and its interaction with light intensity in sweet orange leaf discs under non-photorespiratory conditions. Ciência e Agrotecnologia 30, 670-678.
48. Salvucci M.E. & Crafts-Brandner S.J. (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiology 134, 1460-1470.
49. 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.
50. Schrader S.M., Kleinbeck K.R. & Sharkey T.D. (2007) Rapid heating of intact leaves reveals initial effects of stromal oxidation on photosynthesis. Plant, Cell & Environment 30, 671-678.
51. Schraudner M., Moeder W., Wiese C., Camp W.V., Inzé D., Langebartels C. & Sandermann H., Jr (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. The Plant Journal 16, 235-245.
52. Seemann J.R., Berry J.A. & Downton W.J.S. (1984) Photosynthetic response and adaptation to high temperature in desert plants. A comparison of gas exchange and fluorescence methods for studies of thermal tolerance. Plant Physiology 75, 364-368.
53. 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.
54. Singsaas E.L., Laporte M.M., Shi J.-Z., Monson R.K., Bowling D.R., Johnson K., Lerdau M., Jasentuliytana A. & Sharkey T.D. (1999) Kinetics of leaf temperature fluctuation affect isoprene emission from red oak (Quercus rubra) leaves. Tree Physiology 19, 917-924.
55. Sung D.Y., Kaplan F., Lee K.J. & Guy C.L. (2003) Acquired tolerance to temperature extremes. Trends in Plant Science 8, 179-187.
56. Suzuki N. & Mittler R. (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologia Plantarum 126, 45-51.
57. 0 chlorophyll fluorescence. Plant Physiology 91, 1494-1500.
58. Tian R.-H., Zhang G.-Y., Yan C.-H. & Dai Y.-R. (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Letters 474, 11-15.
59. Tiwari B.S., Belenghi B. & Levine A. (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiology 128, 1271-1281.
60. Tóth S.Z., Schansker G., Kissimon J., Kovács L., Garab G. & Strasser R.J. (2005) Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). Journal of Plant Physiology 162, 181-194.
61. Turner J.G. & Novacky A. (1974) The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 64, 885-890.
62. Vacca R.A., De Pinto M.C., Valenti D., Passarella S., Marra E. & De Gara L. (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco bright-yellow 2 cells. Plant Physiology 134, 1100-1112.
63. Valladares F. & Niinemets Ü. (2007) The architecture of plant crowns: from design rules to light capture and performance. In Handbook of Functional Plant Ecology (eds F.I. Pugnaire & F. Valladares), pp. 101-149. CRC Press, Boca Raton, FL.
64. 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 & Environment 27, 717-724.
65. Wohlgemuth H., Mittelstrass K., Kschieschan S., Bender J., Weigel H.J., Overmyer K., Kangasjärvi J., Sandermann H. & Langebartels C. (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant, Cell & Environment 25, 717-726.
66. Yamada M., Hidaka T. & Fukamachi H. (1996) Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. Scientia Horticulturae 67, 39-48.
67. 0 level and reversible inhibition of photosystem II reaction center by high-temperature treatments in higher plants. Photosynthesis Research 52, 57-64.
68. 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.
69. 0 increases by high temperatures in higher plants. Photosynthesis Research 63, 23-34.
70. Yang C.M. & Heilman J.L. (1993) Response of rice (Oryza sativa L.) to short-term high temperature: growth, development, and yield. Journal of Agricultural Research of China 41, 1-11.
71. Zhang R. & Sharkey T.D. (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynthesis Research 100, 29-43.
72. Zhang R., Cruz J.A., Kramer D.M., Magallanes-Lundback M.E., DellaPenna D. & Sharkey T.D. (2009) Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. Plant, Cell & Environment 32, 1538-1547.
73. Zuppini A., Bugno V. & Baldan B. (2006) Monitoring programmed cell death triggered by mild heat shock in soybean-cultured cells. Functional Plant Biology 33, 617-627.