Photosynthesis Research

, Volume 119, Issue 1–2, pp 101–117 | Cite as

Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation

Review

Abstract

Most plants show considerable capacity to adjust their photosynthetic characteristics to their growth temperatures (temperature acclimation). The most typical case is a shift in the optimum temperature for photosynthesis, which can maximize the photosynthetic rate at the growth temperature. These plastic adjustments can allow plants to photosynthesize more efficiently at their new growth temperatures. In this review article, we summarize the basic differences in photosynthetic reactions in C3, C4, and CAM plants. We review the current understanding of the temperature responses of C3, C4, and CAM photosynthesis, and then discuss the underlying physiological and biochemical mechanisms for temperature acclimation of photosynthesis in each photosynthetic type. Finally, we use the published data to evaluate the extent of photosynthetic temperature acclimation in higher plants, and analyze which plant groups (i.e., photosynthetic types and functional types) have a greater inherent ability for photosynthetic acclimation to temperature than others, since there have been reported interspecific variations in this ability. We found that the inherent ability for temperature acclimation of photosynthesis was different: (1) among C3, C4, and CAM species; and (2) among functional types within C3 plants. C3 plants generally had a greater ability for temperature acclimation of photosynthesis across a broad temperature range, CAM plants acclimated day and night photosynthetic process differentially to temperature, and C4 plants was adapted to warm environments. Moreover, within C3 species, evergreen woody plants and perennial herbaceous plants showed greater temperature homeostasis of photosynthesis (i.e., the photosynthetic rate at high-growth temperature divided by that at low-growth temperature was close to 1.0) than deciduous woody plants and annual herbaceous plants, indicating that photosynthetic acclimation would be particularly important in perennial, long-lived species that would experience a rise in growing season temperatures over their lifespan. Interestingly, across growth temperatures, the extent of temperature homeostasis of photosynthesis was maintained irrespective of the extent of the change in the optimum temperature for photosynthesis (Topt), indicating that some plants achieve greater photosynthesis at the growth temperature by shifting Topt, whereas others can also achieve greater photosynthesis at the growth temperature by changing the shape of the photosynthesis–temperature curve without shifting Topt. It is considered that these differences in the inherent stability of temperature acclimation of photosynthesis would be reflected by differences in the limiting steps of photosynthetic rate.

Keywords

C3 photosynthesis C4 photosynthesis CAM photosynthesis Phenotypic plasticity Temperature acclimation Temperature adaptation 

Supplementary material

11120_2013_9874_MOESM1_ESM.docx (294 kb)
Supplementary material 1 (DOCX 293 kb)
11120_2013_9874_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 18 kb)

References

  1. Atkin OK, Scheurwater I, Pons TL (2006) High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Global Change Biol 12:500–515Google Scholar
  2. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351PubMedGoogle Scholar
  3. Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32:87–105Google Scholar
  4. Barua D, Downs CA, Heckathorn SA (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. Funct Plant Biol 30:1071–1079Google Scholar
  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 Physiol 130:1992–1998PubMedCentralPubMedGoogle Scholar
  6. Bernacchi CJ, Rosenthal DM, Pimentel C, Long SP, Farquhar GD (2009) Modeling the temperature dependence of C3 photosynthesis. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Springer Science + Business Media B.V., Dordrecht, pp 231–246Google Scholar
  7. Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Physiol 31:491–543Google Scholar
  8. Björkman O, Mooney HA, Ehleringer J (1975) Photosynthetic responses of plants from habitats with contrasting thermal environments: comparison of photosynthetic characteristics of intact plants. Carnegie Inst Wash 74:743–748Google Scholar
  9. Borland AM, Griffiths H, Hartwell J, Smith JAC (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. J Exp Bot 60:2879–2896PubMedGoogle Scholar
  10. Brandon PC (1967) Temperature features of enzymes affecting crassulacean acid metabolism. Plant Physiol 42:977–984PubMedCentralPubMedGoogle Scholar
  11. Bukhov NG, 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. Photosynth Res 59:81–93Google Scholar
  12. Bukhov NG, Samson G, Carpentier R (2000) Nonphotosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress: steady-state rate. Photochem Photobiol 72:351–357PubMedGoogle Scholar
  13. Campbell C, Atkinson L, Zaragoza-Castells J, Lundmark M, Atkin OK, Hurry V (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytol 176:375–389PubMedGoogle Scholar
  14. Carter KK (1996) Provenance tests as indicators of growth response to climate change in 10 north temperate tree species. Can J For Res 26:1089–1095Google Scholar
  15. Cen Y-P, Sage RF (2005) The regulation of ribulose-1,5-bisphosphate carboxylase activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:1–12Google Scholar
  16. Chinthapalli B, Murmu J, Raghavendra AS (2003) Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants. J Exp Bot 54:707–714PubMedGoogle Scholar
  17. Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X et al. (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York, pp 847–940Google Scholar
  18. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97:13430–13435PubMedGoogle Scholar
  19. Crafts-Brandner SJ, van de Loo FJ, Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114:439–444PubMedCentralPubMedGoogle Scholar
  20. Cunningham SC, Read J (2002) Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologia 133:112–119Google Scholar
  21. Deiting U, Zrenner R, Stitt M (1998) Similar temperature requirement for sugar accumulation and for the induction of new forms of sucrose phosphate synthase and amylase in cold-stored potato tubers. Plant Cell Environ 21:127–138Google Scholar
  22. Dittrich P (1976) Nicotinamide adenine dinucleotide-specific “Malic” enzyme in Kalanchoe daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiol 57:310–314PubMedCentralPubMedGoogle Scholar
  23. Dittrich P, Campbell WH, Black JRCC (1973) Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiol 52:357–361PubMedCentralPubMedGoogle Scholar
  24. Du Y-C, Nose A, Wasano K (1999) Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species. Plant Cell Environ 22:317–324Google Scholar
  25. Dwyer SA, Ghannoum O, Nicotra A, von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant Cell Environ 30:53–66PubMedGoogle Scholar
  26. Ehleringer JR (1978) Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31:255–267Google Scholar
  27. Ehleringer JR, Björkman O (1977) Quantum yields for CO2 uptake of C3 and C4 plants. Dependence on temperature, CO2 and O2 concentrations. Plant Physiol 59:86–90PubMedCentralPubMedGoogle Scholar
  28. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19Google Scholar
  29. Falcone DL, Ogas JP, Somerville CR (2004) Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol 4:17PubMedCentralPubMedGoogle Scholar
  30. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90PubMedGoogle Scholar
  31. Fischer RA, Edmeades GO (2010) Breeding and cereal yield progress. Crop Sci 50:S85–S98Google Scholar
  32. Furbank RT, Hatch MD (1987) Mechanism of Cq photosynthesis. The size and composition of the inorganic carbon pool in the bundle sheath cells. Plant Physiol 85:958–964PubMedCentralPubMedGoogle Scholar
  33. Furbank RT, Chitty JA, von Caemmerer S, Jenkins CLD (1996) Antisense RNA inhibition of rbcS gene expression reduces Rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol 111:725–734PubMedCentralPubMedGoogle Scholar
  34. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S, Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24:477–485Google Scholar
  35. Genty B, Briantais J-M, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  36. Gombos Z, Wada H, Hideg E, Murata N (1994) The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiol 104:563–567PubMedCentralPubMedGoogle Scholar
  37. Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 99:1443–1448Google Scholar
  38. Havaux M (1996) Short-term responses of photosystem I to heat stress. Photosynth Res 47:85–97PubMedGoogle Scholar
  39. Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444PubMedCentralPubMedGoogle Scholar
  40. Heckathorn SA, Ryan SL, Baylis JA, Wang DF, Hamilton EW III, Cundiff L, Luthe DS (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29:933–944Google Scholar
  41. Hendrickson L, Sharwood R, Ludwig M, Whitney SM, Badger MR, von Caemmerer S (2008) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59:1789–1798PubMedGoogle Scholar
  42. Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494PubMedGoogle Scholar
  43. 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 Cell Physiol 46:1283–1290PubMedGoogle Scholar
  44. Hikosaka K, Murakami A, Hirose T (1999) Balancing carboxylation and regeneration of ribulose bisphosphate in leaf photosynthesis: temperature acclimation in an evergreen tree, Quercus myrsinaefolia. Plant Cell Environ 22:841–849Google Scholar
  45. Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302PubMedGoogle Scholar
  46. Hill RS, Read J, Busby JR (1988) The temperature-dependence of photosynthesis of some Australian temperate rainforest trees and its biogeographical significance. J Biogeogr 15:431–449Google Scholar
  47. Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98:1105–1114PubMedCentralPubMedGoogle Scholar
  48. Huner NPA, Macdowall FDH (1979) Changes in the net charge and subunit properties of ribulose bisphosphate carboxylase-oxygenase during cold hardening of Puma rye. Can J Biochem 57:1036–1041PubMedGoogle Scholar
  49. Hurry VM, Malmberg G, Gardeström P, Öquist G (1994) Effects of a short-term shift to low temperature and of long-term cold hardening on photosynthesis and ribulose 1,5-bisphosphate carboxylase/oxygenase and sucrose phosphate synthase activity in leaves of winter rye (Secale cereale L.). Plant Physiol 106:983–990PubMedCentralPubMedGoogle Scholar
  50. Hurry VM, Strand Å, Tobiæson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol 109:697–706PubMedCentralPubMedGoogle Scholar
  51. Ishikawa K, Onoda Y, Hikosaka K (2007) Intraspecific variation in temperature dependence of gas exchange characteristics of Plantago asiatica ecotypes from different temperature regimes. New Phytol 176:356–364PubMedGoogle Scholar
  52. Jenkins CLD, Furbank RT, Hatch MD (1989) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells. Plant Physiol 91:1356–1363PubMedCentralPubMedGoogle Scholar
  53. Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161:308–313PubMedGoogle Scholar
  54. Kattge J, Knorr W (2007) The temperature dependence of photosynthetic capacity in a photosynthesis model acclimates to plant growth temperature: a re-analysis of data from 36 species. Plant Cell Environ 30:1176–1190PubMedGoogle Scholar
  55. Kingston-Smith AH, Harbinson J, WIlliams J, Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol 114:1039–1046Google Scholar
  56. Kubien DS, Sage RF (2004) Low-temperature photosynthetic performance of a C4 grass and a co-occurring C3 grass native to high latitudes. Plant Cell Environ 27:907–916Google Scholar
  57. Kubien DS, von Cammerer S, Furbank RT, Sage RF (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132:1577–1585PubMedCentralPubMedGoogle Scholar
  58. Kumar A, Li C, Portis Jr. AR (2009) Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynth Res 100:143–153Google Scholar
  59. Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19:3230–3241PubMedCentralPubMedGoogle Scholar
  60. Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173:519–527PubMedGoogle Scholar
  61. Law RD, Crafts-Brandner SJ (2001) High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. Arch Biochem Biophys 386:261–267PubMedGoogle Scholar
  62. 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 214:117–125PubMedGoogle Scholar
  63. Leegood RC, Edwards GE (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic, Dordrecht, pp 191–121Google Scholar
  64. Lobell DB, Asner GP (2003) Climate and management contributions to recent trends in U.S. agricultural yields. Science 299:1032Google Scholar
  65. Long SP (1983) C4 photosynthesis at low temperatures. Plant Cell Environ 6:345–363Google Scholar
  66. Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652PubMedGoogle Scholar
  67. Makino A, Sakuma H, Sudo E, Mae T (2003) Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant Cell Physiol 44:952–956PubMedGoogle Scholar
  68. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedGoogle Scholar
  69. Mooney HA (1980) Photosynthetic plasticity of populations of Heliotropium curassavicum L. Originating from differing thermal regimes. Oecologia (Berl.) 45:372–376Google Scholar
  70. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287:476–479PubMedGoogle Scholar
  71. Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879PubMedCentralPubMedGoogle Scholar
  72. Naidu SL, Moose SP, Al-Shoaibi AK, Raines CA, Long SP (2003) Cold tolerance of C4 photosynthesis in Miscanthus × giganteus: adaptation in amounts and sequence of C4 photosynthetic enzymes. Plant Physiol 132:1688–1697PubMedCentralPubMedGoogle Scholar
  73. Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838PubMedCentralPubMedGoogle Scholar
  74. Nobel P (1996) High productivities of certain agronomic CAM species. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution. Springer-Verlag, Berlin, pp 255–265Google Scholar
  75. Oberhuber WT, Edwards GE (1993) Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiol 101:507–512PubMedCentralPubMedGoogle Scholar
  76. Ogren E, Evans JR (1993) Photosynthetic light-response curves: I. The influence of CO2 partial pressure and leaf inversion. Planta 189:180–190Google Scholar
  77. Ohta S, Ishida Y, Usami S (2006) High-level expression of cold-tolerant pyruvate, orthophosphate dikinase from a genomic clone with site-directed mutations in transgenic maize. Mol Breed 18:29–38Google Scholar
  78. Osborne CP, Wythe EJ, Ibrahim DG, Gilbert ME, Ripley BS (2008) Low temperature effects on leaf physiology and survivorship in the C3 and C4 subspecies of Alloteropsis semialata. J Exp Bot 59:1743–1754PubMedGoogle Scholar
  79. Ow LF, Griffin KL, Whitehead D, Walcroft AS, Turnbull MH (2008) Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoides × nigra. New Phytol 178:123–134PubMedGoogle Scholar
  80. Ow LF, Whitehead D, Walcroft AS, Turnbull M (2010) Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not. Global Change Biol 16:288–302Google Scholar
  81. Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in bean: II CO2 assimilation and metabolite contents. Plant Physiol 112:1253–1260PubMedCentralPubMedGoogle Scholar
  82. Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr.). Plant Physiol 59:795–799PubMedCentralPubMedGoogle Scholar
  83. Pengelly JJL, Tan J, Furbank RT, von Caemmerer S (2012) Antisense reduction of NADP-malic enzyme in Flaveria bidentis reduces flow of CO2 through the C4 cycle. Plant Physiol 160:1070–1080Google Scholar
  84. Pittermann J, Sage RF (2000) Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high-altitude C4 grass from the Rocky Mountains, USA. Plant Cell Environ 23:811–823Google Scholar
  85. Pittermann J, Sage R (2001) The response of the high altitude C4 grass Muhlenbergia montana (Nutt.) A.S. Hitchc. to long- and short-term chilling. J Exp Bot 52:829–838PubMedGoogle Scholar
  86. Price GD, von Caemmerer S, Evans JE, Yu JE, Lloyd L, Oja V, Kell P, Harrison K, Gallagher A, Badger MR (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340Google Scholar
  87. Raines CA (2006) Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. Plant Cell Environ 29:331–339PubMedGoogle Scholar
  88. Read J (1990) Some effects of acclimation temperature on net photosynthesis in some tropical and extra-tropical Australasian Nothofagus species. J Ecol 78:100–112Google Scholar
  89. Read J, Busby JR (1990) Comparative responses to temperature of the major canopy species of Tasmanian cool temperate rainforest and their ecological significance II. Net photosynthesis and climate analysis. Aust J Bot 38:185–205Google Scholar
  90. Reimholz R, Geiger M, Deiting U, Krause KP, Sonnewald U, Stitt M (1997) Potato plants contain multiple forms of sucrose phosphate synthase, that show differences in their tissue distribution, their response during development, and their response to low temperature. Plant Cell Environ 20:291–305Google Scholar
  91. Sage RF (2002) 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 53:609–620PubMedGoogle Scholar
  92. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106PubMedGoogle Scholar
  93. Sage RF, McKown AD (2006) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J Exp Bot 57:303–317PubMedGoogle Scholar
  94. Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84:658–664PubMedCentralPubMedGoogle Scholar
  95. Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. J Exp Bot 59:1581–1595PubMedGoogle Scholar
  96. Salvucci ME, Crafts-Brandner SJ (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol 129:1773–1780PubMedCentralPubMedGoogle Scholar
  97. Salvucci ME, Crafts-Brandner SJ (2004a) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186PubMedGoogle Scholar
  98. Salvucci ME, Crafts-Brandner SJ (2004b) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470PubMedCentralPubMedGoogle Scholar
  99. Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in pima cotton. Plant Cell Environ 27:725–735Google Scholar
  100. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology, and rate limitations. Bot Rev 51:53–105Google Scholar
  101. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, Rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277Google Scholar
  102. Singsaas EL, Sharkey TD (1998) The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant Cell Environ 21:1181–1188Google Scholar
  103. 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. Aust J Plant Physiol 4:583–594Google Scholar
  104. Strand Å, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12:605–614PubMedGoogle Scholar
  105. Strand Å, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperature: increasing cyto-plasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397PubMedCentralPubMedGoogle Scholar
  106. Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8:179–187PubMedGoogle Scholar
  107. Tebaldi C, Hayhoe K, Arblaster JM, Meehl GA (2006) Going to the extremes: an intercomparison of model-simulated historical and future changes in extreme events. Clim Change 79:185–211Google Scholar
  108. Terzaghi WB, Fork DC, Berry JA, Field CB (1989) Low and high temperature limits to PSII. A survey using trans-parinaric acid, delayed light emission, and Fo chlorophyll fluorescence. Plant Physiol 91:1494–1500PubMedCentralPubMedGoogle Scholar
  109. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620Google Scholar
  110. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO publishing, Collingwood, pp 1–165Google Scholar
  111. von Caemmerer S, Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 173–211Google Scholar
  112. von Caemmerer S, Quinn V, Hancock NC, Price GD, Furbank RT, Ludwig M (2004) Carbonic anhydrase and C4 photosynthesis: a transgenic analysis. Plant Cell Environ 27:697–703Google Scholar
  113. von Caemmerer S, Hendrickson L, Quinn V, Vella N, Millgate AG, Furbank RT (2005) Reductions of Rubisco activase by antisense RNA in the C4 plant Flaveria bidentis reduces Rubisco carbamylation and leaf photosynthesis. Plant Physiol 137:747–755Google Scholar
  114. von Caemmerer S, Farquhar GD, Berry JA (2009) Biochemical model of C3 photosynthesis. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Springer Science + Business Media B.V., Dordrecht, pp 209–230Google Scholar
  115. Wagner D (1996) Scenarios of extreme temperature events. Clim Change 33:385–407Google Scholar
  116. Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 5:244–252Google Scholar
  117. Wang D, Naidu SL, Portis AR Jr, Moose SP, Long SP (2008) Can the cold tolerance of C4 photosynthesis in Miscanthus × giganteus relative to Zea mays be explained by differences in activities and thermal properties of Rubisco? J Exp Bot 59:1779–1787PubMedGoogle Scholar
  118. Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688PubMedGoogle Scholar
  119. Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:1066–1081PubMedGoogle Scholar
  120. Way DA, Sage RF (2008a) Elevated growth temperatures reduce the carbon gain of black spruce (Picea mariana (Mill.) B.S.P.). Global Change Biol 14:624–636Google Scholar
  121. Way DA, Sage RF (2008b) Thermal acclimation of photosynthesis in black spruce (Picea mariana (Mill.) B.S.P.). Plant Cell Environ 31:1250–1262PubMedGoogle Scholar
  122. Way DA, Yamori W (2013) Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynth Res. doi:10.1007/s11120-013-9873-7
  123. Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ 27:717–724Google Scholar
  124. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496PubMedGoogle Scholar
  125. 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. Photosynth Res 57:51–59Google Scholar
  126. Yamori W, von Caemmerer S (2009) Effect of Rubisco activase deficiency on the temperature response of CO2 assimilation rate and Rubisco activation state: insights from transgenic tobacco with reduced amounts of Rubisco activase. Plant Physiol 151:2073–2082PubMedCentralPubMedGoogle Scholar
  127. 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 Environ 28:536–547Google Scholar
  128. Yamori W, Noguchi K, Hanba YT, Terashima I (2006a) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Physiol 47:1069–1080PubMedGoogle Scholar
  129. Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006b) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29:1659–1670PubMedGoogle Scholar
  130. Yamori W, Noguchi K, Kashino Y, Terashima I (2008) The role of electron transport in determining the temperature dependence of the photosynthetic rate in spinach leaves grown at contrasting temperatures. Plant Cell Physiol 49:583–591PubMedGoogle Scholar
  131. Yamori W, Noguchi K, Hikosaka K, Terashima I (2009) Cold-tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold-sensitive species. Plant Cell Physiol 50:203–215PubMedGoogle Scholar
  132. Yamori W, Evans JR, von Caemmerer S (2010a) Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation rate in tobacco leaves. Plant Cell Environ 33:332–343PubMedGoogle Scholar
  133. Yamori W, Noguchi K, Hikosaka K, Terashima I (2010b) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152:388–399PubMedCentralPubMedGoogle Scholar
  134. Yamori W, Nagai T, Makino A (2011a) The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species. Plant Cell Environ 34:764–777PubMedGoogle Scholar
  135. Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (2011b) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68:966–976PubMedGoogle Scholar
  136. Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S (2011c) The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol 155:956–962PubMedCentralPubMedGoogle Scholar
  137. Yamori W, Masumoto C, Fukayama H, Makino A (2012) Rubisco activase is a key regulator of non steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J 71:871–880PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Wataru Yamori
    • 1
  • Kouki Hikosaka
    • 2
    • 3
  • Danielle A. Way
    • 4
    • 5
  1. 1.Center for Environment, Health and Field SciencesChiba UniversityKashiwaJapan
  2. 2.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  3. 3.CREST, JSTTokyoJapan
  4. 4.Department of BiologyUniversity of Western OntarioLondonCanada
  5. 5.Nicholas School of the EnvironmentDuke UniversityDurhamUSA

Personalised recommendations