Temperature acclimation of photosynthesis: Mechanisms involved in the changes in temperature dependence of photosynthetic rate

Journal of Experimental Botany

Volumn 57, Issue 2 SPEC. ISS., 2006, Pages 291-302

  Hikosaka, Kouki ^a   Ishikawa, Kazumasa ^a   Borjigidai, Almaz ^a   Muller, Onno ^a   Onoda, Yusuke ^a,b  

^a TOHOKU UNIVERSITY   (Japan)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Activation energy; Gas exchange; Limitation; Limiting step; Model; Nitrogen use; Optimal temperature; Photosynthetic acclimation; Temperature response

Indexed keywords

ACTIVATION ENERGY; BIOCHEMICAL ENGINEERING; CELLS; CONCENTRATION (PROCESS); PARAMETER ESTIMATION; TEMPERATURE MEASUREMENT;

GAS EXCHANGE; LIMITATION; LIMITING STEP; NITROGEN USE; OPTIMAL TEMPERATURE; PHOTOSYNTHETIC ACCLIMATION; TEMPERATURE RESPONSE;

PHOTOSYNTHESIS;

CARBON DIOXIDE; NITROGEN; RIBULOSE PHOSPHATE; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ACCLIMATIZATION; CONFERENCE PAPER; CYTOLOGY; GREENHOUSE EFFECT; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; PLANT PHYSIOLOGY; TEMPERATURE;

ACCLIMATIZATION; CARBON DIOXIDE; GREENHOUSE EFFECT; KINETICS; NITROGEN; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PHYSIOLOGY; RIBULOSE-BISPHOSPHATE CARBOXYLASE; RIBULOSEPHOSPHATES; TEMPERATURE;

EID: 30344449159     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erj049     Document Type: Conference Paper

References (89)

1. Armond PA, 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.
2. Badger MR, Björkman O, Armond PA. 1982. An analysis of photosynthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant, Cell and Environment 5, 85-99.
3. Battaglia M, Beadle C, Loughhead S. 1996. Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. Tree Physiology 16, 81-89.
4. Bernacchi CJ, Singsaas EL, Pimentel C, Portis Jr AR, Long SP. 2001. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell and Environment 24, 253-259.
5. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP. 2002. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 130, 1992-1998.
6. Berry J, Björkman O. 1980. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491-543.
7. Billings WD, Godfrey PJ, Chabot BF, Bourque DP. 1971. Metabolic acclimation to temperature in arctic and alpine ecotypes of Oxyria digyna. Arctic and Alpine Research 3, 277-289.
8. Boardman NK. 1977. Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28, 355-377.
9. 2 specificity of ribulose-1,5-bisphosphate carboxylase and the relationship to photosynthesis. Plant Physiology 74, 759-765.
10. Bunce JA. 1998. The temperature dependence of the stimulation of photosynthesis by elevated carbon dioxide in wheat and barley. Journal of Experimental Botany 49, 1555-1561.
11. 3 species: temperature dependence of parameters of a biochemical photosynthesis model. Photosynthesis Research 63, 59-67.
12. Chow WS, Anderson JM. 1987. Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. II. Thylakoid membrane components. Australian Journal of Plant Physiology 14, 9-19.
13. 2. Proceedings of the National Academy of Sciences, USA 97, 13430-43435.
14. Cunningham SC, Read J. 2002. Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologia 133, 112-119.
15. Evans JR. 1987. The relationship between electron transport components and photosynthetic capacity in pea leaves grown at different irradiances. Australian Journal of Plant Physiology 14, 69-79.
16. 3 plants. Oecologia 78, 9-19.
17. Evans JR, von Caemmerer S. 1996. Carbon dioxide diffusion inside leaves. Plant Physiology 110, 339-346.
18. 3 plants. Planta 149, 78-90.
19. Farquhar GD, von Caemmerer S. 1982. Modelling of photosynthetic response to environment. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encyclopedia of plant physiology, New series, Vol. 12B. Berlin: Springer-Verlag, 549-587.
20. Feller U, Crafts-Brandner SJ, Salvucci ME. 1998. Moderately high temperatures inhibit ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiology 116, 539-546.
21. Ferrar PJ, Slatyer RO, Vranjic JA. 1989. Photosynthetic temperature acclimation in Eucalyptus species from diverse habitats and a comparison with Nerium oleander. Australian Journal of Plant Physiology 16, 199-217.
22. Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ. 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell and Environment 28, 571-579.
23. Gunderson CA, Norby RJ, Wullschleger SD. 2000. Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiology 20, 87-95.
24. Gutteridge S, Gatenby AA. 1995. Rubisco synthesis, assembly, mechanism, and regulation. The Plant Cell 7, 809-819.
25. 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, 302-317.
26. Han Q, Kawasaki T, Nakano T, Chiba Y. 2004. Spatial and seasonal variability of temperature responses of biochemical photosynthesis parameters and leaf nitrogen content within a Pinus densiflora crown. Tree Physiology 24, 737-744.
27. 3 leaves to environmental factors. In: Boote KJ, Loomis RS, eds. Modelling crop photosynthesis: from biochemistry to canopy. Madison, WI: CSSA, 17-39.
28. 2. Plant Physiology 98, 1429-1436.
29. 2. Plant, Cell and Environment 15, 271-282.
30. Hendrickson L, Ball MC, Wood JT, Chow WS, Furbank RT. 2004. Low temperature effects on photosynthesis and growth of grapevine. Plant, Cell and Environment 27, 795-809.
31. Hikosaka K. 1996. Effects of leaf age, nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Planta 198, 144-150.
32. 3 plants with respect to nitrogen use. Annals of Botany 80, 721-730.
33. Hikosaka K. 2004. Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research 117, 481-494.
34. Hikosaka K. 2005. Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown at different temperature and light conditions: similarities and differences between temperature and light acclimation. Plant and Cell Physiology 46, 1283-1290.
35. Hikosaka K, Hirose T. 2001. Temperature acclimation of the photosynthetic apparatus in an evergreen shrub, Nerium oleander. In: PS2001 Proceedings of the 12th International Congress on Photosynthesis. Melbourne: CSIRO Publishing, S35-007.
36. Hikosaka K, Murakami A, Hirose T. 1999. Balancing carboxylation and regeneration of ribulose-1,5-bisphosphate in leaf photosynthesis in temperature acclimation of an evergreen tree, Quercus myrsinaefolia. Plant, Cell and Environment 22, 841-849.
37. 3 plants to sun and shade with respect to nitrogen use. Plant, Cell and Environment 18, 605-618.
38. Hikosaka K, Terashima I. 1996. Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Functional Ecology 10, 335-343.
39. Hirose T. 1984. Nitrogen use efficiency in growth of Polygonum cuspidatum Sieb. et Zucc. Annals of Botany 54, 695-704.
40. Hirose T, Werger MJA. 1987. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of Solidago altissima stand. Physiologia Plantarum 70, 215-222.
41. Holaday AS, Martindale W, Aired R, Brooks AL, Leegood RC. 1992. Changes in activities of enzymes of carbon metabolisms in leaves during exposure of plants to low temperature. Plant Physiology 98, 1105-1114.
42. Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M. 1993. Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynthesis Research 37, 19-39.
43. Huner NPA, Öquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224-230.
44. Johnson F, Erying H, Williams R. 1942. The nature of enzyme inhibitions in bacterial luminescence: sulphanilamide, urethane, temperature, pressure. Journal of Cell and Comparative Physiology 20, 247-268.
45. 2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161, 308-313.
46. Kanechi M, Uchida N, Yasuda T, Yamaguchi T. 1996. Non-stomatal inhibition associated with inactivation of Rubisco in dehydrated coffee leaves under unshaded and shaded conditions. Plant and Cell Physiology 37, 455-460.
47. Kirschbaum MUF, Farquhar GD. 1984. Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Australian Journal of Plant Physiology 11, 519-538.
48. Kobza J, Edwards GE. 1987. Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69-74.
49. Labate CA, Leegood RC. 1988. Limitation of photosynthesis by changes in temperature. Planta 173, 519-527.
50. Law RD, Crafts-Brandner SJ. 1999. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173-181.
51. Law RD, Crafts-Brandner SJ, Salvucci ME. 2001. Heat stress induces the synthesis of a new form of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in cotton leaves. Planta 214, 117-125.
52. 3 plants. Plant, Cell and Environment 18, 339-355.
53. Leuning R. 2002. Temperature dependence of two parameters in a photosynthesis model. Plant, Cell and Environment 25, 1205-1210.
54. Makino A, Nakano H, Mae T. 1994. Effects of growth temperature on the responses of ribulose-1,5-bisphosphate carboxylase, electron transport components, and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis. Plant Physiology 105, 1231-1238.
55. Makino A, Sato T, Nakano H, Mae T. 1997. Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta 203, 390-398.
56. Medlyn BR, Dreyer E, Ellsworth D, et al. 2002b. Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant Cell and Environment 25, 1167-1179.
57. Medlyn BE, Loustau D, Delzon S. 2002a. Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant, Cell and Environment 25, 1155-1165.
58. Mitchell RAC, Barber J. 1986. Adaptation of photosynthetic electron-transport rate to growth temperature in pea. Planta 169, 429-436.
59. Mooney HA, Björkman O, Collatz GJ. 1978. Photosynthetic acclimation to temperature in the desert shrub, Larrea divancata. I. Carbon dioxide exchange characteristics of intact leaves. Plant Physiology 61, 406-410.
60. Muller O, Hikosaka K, Anten NPR, Hirose T, Werger MJA. 2005b. Optimal leaf nitrogen content of an evergreen understorey plant in a temperate climate. In: van der Est A, Bruce D, eds. Photosynthesis: fundamental aspects to global perspectives. Lawrence, KS: Allen Press, 636-638.
61. Muller O, Hikosaka K, Hirose T. 2005a. Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understorey. Oecologia 143, 501-508.
62. 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 and Environment 22, 1497-1513.
63. 2 response of photosynthesis in Polygonum cuspidatum. Journal of Experimental Botany 56, 755-763.
64. Onoda Y, Hikosaka K, Hirose T. 2005b. The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature. Functional Plant Biology 32, 903-910.
65. Perchorowicz JT, Raynes DA, Jensen RG. 1981. Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proceedings of the National Academy of Sciences, USA 78, 2985-2989.
66. Rustad LE, Campbell J, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J. 2001. A meta-analysis of the response of soil respiration, net N mineralization, and above-ground plant growth to experimental ecosystem warming. Oecologia 126, 543-562.
67. 3 plants. Plant Physiology 94, 1728-1734.
68. 2: the gas exchange perspective. Photosynthesis Research 39, 351-368.
69. 2 enrichment. Vegetatio 121, 67-77.
70. 2 in Phaseolus vulgaris L. Planta 174, 407-416.
71. Salvucci ME, Crafts-Brandner SJ. 2004a. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120, 179-186.
72. Salvucci ME, Crafts-Brandner SJ. 2004b. Mechanisms for deactivation of Rubisco under moderate heat stress. Physiologia Plantarum 122, 513-519.
73. Salvucci ME, Crafts-Brandner SJ. 2004c. 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.
74. 3 plants: physics, physiology, and rate limitations. Botanical Review 51, 53-105.
75. Slatyer RO. 1977. Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. IV. Temperature response of four populations grown at different temperatures. Australian Journal of Plant Physiology 4, 583-594.
76. Smith EM, Hadley EB. 1974. Photosynthetic and respiratory acclimation to temperature in Ledum groenlandicum populations. Arctic and Alpine Research 6, 13-27.
77. Steffen KL, Wheeler RM, Arora R, Palta JP, Tibbitts TW. 1995. Balancing photosynthetic light-harvesting and light-utilization capacities in potato leaf tissue during acclimation to different growth temperatures. Physiologia Plantarum 94, 51-56.
78. Strand Å, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M. 1999. Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiology 119, 1387-1397.
79. Terashima I, Evans JR. 1988. Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant and Cell Physiology 29, 143-155.
80. Terashima I, Araya T, Miyazawa SI, Sone K, Yano S. 2005. Construction and maintenance of the optimal photosynthetic system of the leaf, herbaceous plant and tree: an eco-developmental treatise. Annals of Botany 95, 507-519.
81. von Caemmerer S. 2000. Biochemical models of leaf photosynthesis. Canberra, Australia: CSIRO Publishing.
82. 3 plants. Australian Journal of Plant Physiology 18, 287-305.
83. von Caemmerer S, Evans JR, Hudson GS, Andrews TJ. 1994. The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195, 88-87.
84. von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153, 376-387.
85. Weis E. 1981. Reversible heat-inactivation of the Calvin Cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151, 33-39.
86. Williams DG, Black RA. 1993. Phenotypic variation in contrasting temperature environments: growth and photosynthesis in Pennisetum setaceum from different altitudes on Hawaii. Functional Ecology 7, 623-633.
87. i curves from 109 species. Journal of Experimental Botany 44, 907-920.
88. Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S. 2002. Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiology 128, 1087-1097.
89. Yamori W, Noguchi K, Terashima I. 2005. Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant, Cell and Environment 28, 536-547.