Photosynthesis Research

, Volume 119, Issue 1–2, pp 89–100 | Cite as

Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration

Review

Abstract

While interest in photosynthetic thermal acclimation has been stimulated by climate warming, comparing results across studies requires consistent terminology. We identify five types of photosynthetic adjustments in warming experiments: photosynthesis as measured at the high growth temperature, the growth temperature, and the thermal optimum; the photosynthetic thermal optimum; and leaf-level photosynthetic capacity. Adjustments of any one of these variables need not mean a concurrent adjustment in others, which may resolve apparently contradictory results in papers using different indicators of photosynthetic acclimation. We argue that photosynthetic thermal acclimation (i.e., that benefits a plant in its new growth environment) should include adjustments of both the photosynthetic thermal optimum (Topt) and photosynthetic rates at the growth temperature (Agrowth), a combination termed constructive adjustment. However, many species show reduced photosynthesis when grown at elevated temperatures, despite adjustment of some photosynthetic variables, a phenomenon we term detractive adjustment. An analysis of 70 studies on 103 species shows that adjustment of Topt and Agrowth are more common than adjustment of other photosynthetic variables, but only half of the data demonstrate constructive adjustment. No systematic differences in these patterns were found between different plant functional groups. We also discuss the importance of thermal acclimation of respiration for net photosynthesis measurements, as respiratory temperature acclimation can generate apparent acclimation of photosynthetic processes, even if photosynthesis is unaltered. We show that while dark respiration is often used to estimate light respiration, the ratio of light to dark respiration shifts in a non-predictable manner with a change in leaf temperature.

Keywords

Temperature acclimation Carbon balance Global change biology Meta-analysis Day respiration 

Supplementary material

11120_2013_9873_MOESM1_ESM.docx (66 kb)
Supplementary material 1 (DOCX 67 kb)

References

  1. Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111PubMedCentralCrossRefGoogle Scholar
  2. Atkin OK, Evans JR, Ball MC, Lambers H, Pons TL (2000) Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiol 122:915–923PubMedCentralPubMedCrossRefGoogle Scholar
  3. 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 congener. Glob Chang Biol 12:500–515CrossRefGoogle Scholar
  4. Atkin OK, Scheurwater I, Pons TL (2007) Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures. New Phytol 174:367–380PubMedCrossRefGoogle Scholar
  5. Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impact of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial age atmospheric growth CO2 and temperature. New Phytol 190:1003–1018PubMedCrossRefGoogle Scholar
  6. Badger MR, Bjorkman O, Armond PA (1982) An analysis of photosynthetic temperature response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant, Cell Environ 5:85–99Google Scholar
  7. Bauerle WL, Bowden JD, Wang GG (2007) The influence of temperature on within-canopy acclimation and variation in leaf photosynthesis: spatial acclimation to microclimate gradients among climatically divergent Acer rubrum L. genotypes. J Exp Bot 58:3285–3298PubMedCrossRefGoogle Scholar
  8. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543CrossRefGoogle Scholar
  9. Bronson DR, Gower ST (2010) Ecosystem warming does not affect photosynthesis or aboveground autotrophic respiration for boreal black spruce. Tree Physiol 30:441–449PubMedCrossRefGoogle Scholar
  10. Campbell GS, Norman JM (1998) An introduction to environmental biophysics, 2nd edn. Springer, New York, p 286CrossRefGoogle Scholar
  11. Campbell C, Atkinson L, Zaragoza-Castells J, Lundmark M, Atkin O, Hurry V (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional type. New Phytol 176:375–389PubMedCrossRefGoogle Scholar
  12. Centritto M, Brilli F, Fodale R, Loreto F (2011) Different sensitivity of isoprene emission, respiration and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra) saplings. Tree Physiol 31:275–286PubMedCrossRefGoogle Scholar
  13. Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (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/New YorkGoogle Scholar
  14. Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell Environ 21:427–435CrossRefGoogle Scholar
  15. Dillaway DN, Kruger EL (2010) Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect. Plant, Cell Environ 33:888–899CrossRefGoogle Scholar
  16. Dwyer SA, Ghannoum O, Nicotra A, von Cammerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant, Cell Environ 30:53–66CrossRefGoogle Scholar
  17. Fares S, Mahmood T, Liu S, Loreto F, Centritto M (2011) Influence of growth temperature and measuring temperature on isoprene emission, diffusive limitations of photosynthesis and respiration in hybrid poplars. Atmos Environ 45:155–161CrossRefGoogle Scholar
  18. Ferrar PJ, Slatyer RO, Vranjic JA (1989) Photosynthetic temperature acclimation in Eucalyptus species from diverse habitats, and a comparison with Nerium oleander. Aust J Plant Physiol 16:199–217CrossRefGoogle Scholar
  19. Ghannoum O, Phillips NG, Sears MA, Logan BA, Lewis JD, Conroy JP, Tissue DT (2010) Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ 33:1671–1681PubMedCrossRefGoogle Scholar
  20. Gunderson CA, O’Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Chang Biol 16:2272–2286CrossRefGoogle Scholar
  21. 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 Environ 28:302–317CrossRefGoogle Scholar
  22. Hikosaka K, Murakami A, Hirose T (1999) Balancing carboxylation and regeneration of ribulose-1,5-bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia. Plant Cell Environ 22:841–849CrossRefGoogle Scholar
  23. Hurry V, Igamberdiev AU, Keerberg O, Parnik T, Atkin OK, Zaragoza-Castells J, Gardestrom P (2005) Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem. Kluwer, DordrechtGoogle Scholar
  24. Ishikawa K, Onoda Y, Hikosaka K (2007) Intraspecific variation in temperature dependence of gas exchange characteristics among Plantago asiatica ecotypes from different temperature regimes. New Phytol 176:356–364PubMedCrossRefGoogle Scholar
  25. Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant, Cell Environ 30:1176–1190CrossRefGoogle Scholar
  26. Kok B (1948) A critical consideration of the quantum yield of Chlorella photosynthesis. Enzymologia 13:1–56Google Scholar
  27. Kositsup B, Montpied P, Kasemsap P, Thaler P, Ameglio T, Dreyer E (2009) Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Mull. Arg.) acclimate to changes in ambient temperature. Trees 23:357–365CrossRefGoogle Scholar
  28. Laisk AK (1977) Kinetics of photosynthesis and photorespiration in C3 plants. Nauka, MoscowGoogle Scholar
  29. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876PubMedCrossRefGoogle Scholar
  30. Lewis JD, Lucash M, Olszyk DM, Tingey DT (2004) Relationships between needle nitrogen concentration and photosynthetic responses of Douglas-fir seedlings to elevated CO2 and temperature. New Phytol 162:355–364CrossRefGoogle Scholar
  31. Mawson BT, Svoboda J, Cummins RW (1986) Thermal acclimation of photosynthesis by the arctic plant Saxifraga cernua. Can J Bot 64:71–76CrossRefGoogle Scholar
  32. Niu S, Luo Y, Fei S, Yuan W, Schimel D, Law BE, Ammann C et al (2012) Thermal optimality of net ecosystem exchange of carbon dioxide and underlying mechanisms. New Phytol 194:775–783PubMedCrossRefGoogle Scholar
  33. Ow LF, Griffin KL, Whitehead D, Walcroft AS, Turnbull MH (2008a) Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoides × nigra. New Phytol 178:123–134PubMedCrossRefGoogle Scholar
  34. Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2008b) Thermal acclimation of respiration but not photosynthesis in Pinus radiata. Funct Plant Biol 35:448–461CrossRefGoogle Scholar
  35. Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2010) Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not. Glob Chang Biol 16:288–302CrossRefGoogle Scholar
  36. Pons TL (2012) Interaction of temperature and irradiance effects on photosynthetic acclimation in two accessions of Arabidopsis thaliana. Photosynth Res 1–3:207–219CrossRefGoogle Scholar
  37. Rilkonen J, Maenpaa M, Alavillamo M, Silfver T, Oksanen E (2009) Interactive effect of elevated temperature and O3 on antioxidant capacity and gas exchange in Betula pendula saplings. Planta 230:419–427CrossRefGoogle Scholar
  38. Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2—the gas exchange perspective. Photosynth Res 39:351–368PubMedCrossRefGoogle Scholar
  39. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106PubMedCrossRefGoogle Scholar
  40. Scafaro AP, Yamori W, Carmo-Silva AE, Salvucci ME, von Caemmerer S, Atwell BJ (2012) Rubisco activity is associated with photosynthetic thermotolerance in a wild rice (Oryza meridionalis). Physiol Plant 146:99–109PubMedCrossRefGoogle Scholar
  41. Shen H, Klein JA, Zhao X, Tang Y (2009) Leaf photosynthesis and simulated carbon budget of Gentiana straminea from a decade-long warming experiment. J Plant Ecol 2:207–216CrossRefGoogle Scholar
  42. Silim SN, Ryan N, Kubien DS (2010) Temperature responses of photosynthesis and respiration in Populus balsamifera L.: acclimation versus adaptation. Photosynth Res 104:19–30PubMedCrossRefGoogle Scholar
  43. Stirling CM, Davey PA, Williams TG, Long SP (1997) Acclimation of photosynthesis to elevated CO2 and temperature in five British native species of contrasting functional type. Glob Chang Biol 3:237–246CrossRefGoogle Scholar
  44. Suwa R, Hakata H, Hara H, El-Shemy HA, Adu-Gyamfi JJ, Nguyen NT, Kanai S, Lightfoot DA, Mohapatra K, Fujita K (2010) High temperature effects on photosynthate partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes. Plant Physiol Biochem 48:124–130PubMedCrossRefGoogle Scholar
  45. Turnbull MH, Murthy R, Griffin KL (2002) The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides. Plant Cell Environ 25:1729–1737CrossRefGoogle Scholar
  46. Wang K-Y, Kellomaki S, Laitinen K (1996) Acclimation of photosynthetic parameters in Scots pine after three years exposure to elevated temperature and CO2. Agric For Meteorol 82:195–217CrossRefGoogle Scholar
  47. Warren CR (2008) Does growth temperature affect the temperature responses of photosynthesis and internal conductance to CO2? A test with Eucalyptus regnans. Tree Physiol 28:11–19PubMedCrossRefGoogle Scholar
  48. 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 30:669–688PubMedCrossRefGoogle Scholar
  49. Way DA, Sage RF (2008a) Elevated growth temperatures reduce the carbon gain of black spruce (Picea mariana (Mill.) B.S.P.). Glob Chang Biol 14:624–636CrossRefGoogle Scholar
  50. Way DA, Sage RF (2008b) Thermal acclimation of photosynthesis in black spruce (Picea mariana (Mill.) B.S.P.). Plant Cell Environ 31:1250–1262PubMedCrossRefGoogle Scholar
  51. Wertin TM, McGuire MA, Teskey RO (2010) Higher growth temperatures decreased net carbon assimilation and biomass accumulation of northern red oak seedlings near the southern limit of the species range. Tree Physiol 30:1277–1288Google Scholar
  52. Whitney SM, Houtz RL, Alonso H (2011a) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol 155:27–35PubMedCentralPubMedCrossRefGoogle Scholar
  53. Whitney SM, Sharwood RE, Orr D, White SJ, Alonso H, Galmes J (2011b) Isoleucine 309 acts as a C-4 catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria. Proc Natl Acad Sci USA 108:14688–14693PubMedCrossRefGoogle Scholar
  54. Wolf S, Olesinski AA, Rudich J, Marani A (1990) Effect of high temperature on photosynthesis in potato. Ann Bot 65:179–185Google Scholar
  55. Xiong FS, Mueller EC, Day TA (2000) Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. Am J Bot 87:700–710PubMedCrossRefGoogle Scholar
  56. 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 28:536–537CrossRefGoogle Scholar
  57. Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006) 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 29:1659–1670PubMedCrossRefGoogle Scholar
  58. 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 49:583–591PubMedCrossRefGoogle Scholar
  59. Yamori W, Noguchi K, Hikosaka K, Terashima I (2009) Cold-tolerant crops have greater temperature homeostasis of leaf respiration and photosynthesis than cold-sensitive species. Plant Cell Physiol 50:203–215PubMedCrossRefGoogle Scholar
  60. Yamori W, Noguchi K, Hikosaka K, Terashima I (2010) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152:388–399PubMedCentralPubMedCrossRefGoogle Scholar
  61. Yamori W, Hikosaka K, Way DA (2013) Temperature response of photosynthesis in C3, C4 and CAM plants: temperature acclimation versus temperature adaptation. Photosynth Res. doi:10.1007/s11120-013-9874-6
  62. Zaragoza-Castells J, Sanchez-Gomez D, Valladares F, Hurry V, Atkin OK (2007) Does growth irradiance affect temperature dependence and thermal acclimation of leaf respiration? Insights from a Mediterranean tree with long-lived leaves. Plant Cell Environ 30:820–833PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiologyWestern UniversityLondonCanada
  2. 2.Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  3. 3.Center for Environment, Health and Field SciencesChiba UniversityKashiwaJapan

Personalised recommendations