Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Evans Review No. 2: The hot and the cold: unravelling the variable response of plant respiration to temperature

Owen K. Atkin A , Dan Bruhn B , Vaughan M. Hurry C and Mark G. Tjoelker D
+ Author Affiliations
- Author Affiliations

A Department of Biology (Area 2), The University of York, PO Box 373, York YO10 5YW, UK. Corresponding author. Email: OKA1@york.ac.uk

B Cooperative Research Centre for Green House Accounting, Ecosystem Dynamics Group, Research School of Biological Sciences, Australian National University, Canberra, ACT 0200, Australia.

C Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 901 87 Umeå, Sweden.

D Department of Forest Science, Texas A & M University, 2135 TAMU, College Station, TX 77843-2135, USA.

This paper is part of The Evans Review series, named for Dr Lloyd Evans. The series contains reviews that are critical, state-of-the-art evaluations that aim to advance our understanding, rather than being exhaustive compilations of information, and are written by invitation.

Functional Plant Biology 32(2) 87-105 https://doi.org/10.1071/FP03176
Submitted: 30 September 2003  Accepted: 14 December 2004   Published: 24 February 2005

Abstract

When predicting the effects of climate change, global carbon circulation models that include a positive feedback effect of climate warming on the carbon cycle often assume that (1) plant respiration increases exponentially with temperature (with a constant Q10) and (2) that there is no acclimation of respiration to long-term changes in temperature. In this review, we show that these two assumptions are incorrect. While Q10 does not respond systematically to elevated atmospheric CO2 concentrations, other factors such as temperature, light, and water availability all have the potential to influence the temperature sensitivity of respiratory CO2 efflux. Roots and leaves can also differ in their Q10 values, as can upper and lower canopy leaves. The consequences of such variable Q10 values need to be fully explored in carbon modelling. Here, we consider the extent of variability in the degree of thermal acclimation of respiration, and discuss in detail the biochemical mechanisms underpinning this variability; the response of respiration to long-term changes in temperature is highly dependent on the effect of temperature on plant development, and on interactive effects of temperature and other abiotic factors (e.g. irradiance, drought and nutrient availability). Rather than acclimating to the daily mean temperature, recent studies suggest that other components of the daily temperature regime can be important (e.g. daily minimum and / or night temperature). In some cases, acclimation may simply reflect a passive response to changes in respiratory substrate availability, whereas in others acclimation may be critical in helping plants grow and survive at contrasting temperatures. We also consider the impact of acclimation on the balance between respiration and photosynthesis; although environmental factors such as water availability can alter the balance between these two processes, the available data suggests that temperature-mediated differences in dark leaf respiration are closely linked to concomitant differences in leaf photosynthesis. We conclude by highlighting the need for a greater process-based understanding of thermal acclimation of respiration if we are to successfully predict future ecosystem CO2 fluxes and potential feedbacks on atmospheric CO2 concentrations.

Keywords: carbon fluxes, climate change, respiration, temperature.


Acknowledgments

This work was supported by grants from NERC in the UK (GR3/11898, NERC/A/S/2001/01186, NERC/B/S/2001/00875; OKA), the National Science Foundation (USA, IBN-9630241; MGT) the Swedish Council for Forestry and Agricultural Research (VH), The Cooperative Research Centre for Greenhouse Accounting, Australia (DB), and the Nordic Academy of Advanced Studies (NorFA) Temperature Stress Network.


References


Aber JD, Federer CA (1992) A generalized, lumped-parameter model of photosynthesis, evapotranspiration and net primary production in temperate and boreal forest ecosystems. Oecologia 92, 463–474.
CrossRef | open url image1

Amthor, JS (1997). Plant respiratory response to elevated CO2 partial pressure. In ‘Advances in carbon dioxide effects research’. pp. 35–77. (American Society of Agronomy: Wisconsin)

Amthor JS (2000) The McCree-de Wit–Penning de Vries–Thornley respiration paradigms, 30 years later. Annals of Botany 86, 1–20.
CrossRef | open url image1

Arnone JA, Körner C (1997) Temperature adaptation and acclimation potential of leaf dark respiration in two species of Ranunculus from warm and cold habitats. Arctic and Alpine Research 29, 122–125. open url image1

Atkin OK, Day DA (1990) A comparison of the respiratory processes and growth rates of selected Australian alpine and related lowland plant species. Australian Journal of Plant Physiology 17, 517–526. open url image1

Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
CrossRef | PubMed | open url image1

Atkin OK, Botman B, Lambers H (1996) The causes of inherently slow growth in alpine plants: an analysis based on the underlying carbon economies of alpine and lowland Poa species. Functional Ecology 10, 698–707. open url image1

Atkin OK, Edwards EJ, Loveys BR (2000a) Response of root respiration to changes in temperature and its relevance to global warming. New Phytologist 147, 141–154.
CrossRef | open url image1

Atkin OK, Holly C, Ball MC (2000b) 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 and Environment 23, 15–26.
CrossRef | open url image1

Atkin OK, Evans JR, Ball MC, Pons TL, Lambers H (2000c) Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiology 122, 915–923.
CrossRef | PubMed | open url image1

Atkin, OK , Millar, AH , Gardeström, P ,  and  Day, DA (2000d). Photosynthesis, carbohydrate metabolism and respiration in leaves of higher plants. In ‘Photosynthesis, physiology and metabolism’. d. pp. 153–175. (Kluwer Academic Publishers: Dordrecht)

Atkin OK, Zhang QS, Wiskich JT (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.
CrossRef | PubMed | open url image1

Azcón-Bieto, J (1992). Relationships between photosynthesis and respiration in the dark in plants. In ‘Trends in photosynthesis research’. pp. 241–253. (Intercept Ltd: Andover)

Azcón-Bieto J, Gonzalelz-Meler MA, Doherty W, Drake B (1994) Acclimation of respiratory O2 uptake in green tissues of field-grown native species after long-term exposure to elevated atmospheric CO2. Plant Physiology 106, 1163–1168.
PubMed |
open url image1

Berry, JA ,  and  Raison, JK (1981). Responses of macrophytes to temperature. In ‘Physiological plant ecology I. Responses to the physical environment’. pp. 277–338. (Springer-Verlag: Berlin)

Bigot J, Boucaud J (1996) Short-term responses of Brassica rapa plants to low root temperature, effects on nitrate uptake and its translocation to the shoot. Physiologia Plantarum 96, 646–654.
CrossRef | open url image1

Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biological Reviews 43, 481–529. open url image1

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. open url image1

Bolstad PV, Mitchell K, Vose JM (1999) Foliar temperature-respiration response functions for broad-leaved tree species in the southern Appalachians. Tree Physiology 19, 871–878.
PubMed |
open url image1

Bolstad PV, Reich P, Lee T (2003) Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra. Tree Physiology 23, 969–976.
PubMed |
open url image1

Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396, 570–572.
CrossRef | open url image1

Bouma TJ, Nielsen KL, Eissenstat DM, Lynch JP (1997) Estimating respiration of roots in soil, interactions with soil CO2, soil temperature and soil water content. Plant and Soil 195, 221–232.
CrossRef | open url image1

Brooks A, Farquhar GD (1985) Effect of temperature on the CO2–O2 specificity of ribulose-1,5-biphosphate carboxylase / oxygenase and the rate of respiration in the light. Estimates from gas exchange measurements on spinach. Planta 165, 397–406.
CrossRef | open url image1

Bruhn D (2002) Plant pespiration and climate change effects. PhD thesis. (Risø National Laboratory, Roskilde: Denmark)

Bruhn D, Mikkelsen TN, Atkin OK (2002) Does the direct effect of atmospheric CO2 concentration on leaf respiration vary with temperature? Responses in two species of Plantago that differ in relative growth rate. Physiologia Plantarum 114, 57–64.
CrossRef | PubMed | open url image1

Bryla DR, Bouma TJ, Eissenstat DM (1997) Root respiration in citrus acclimates to temperature and slows during drought. Plant, Cell and Environment 20, 1411–1420.
CrossRef | open url image1

Bryla DR, Bouma TJ, Hartmond U, Eissenstat DM (2001) Influence of temperature and soil drying on respiration of individual roots in citrus, integrating greenhouse observations into a predictive model for the field. Plant, Cell and Environment 24, 781–790.
CrossRef | open url image1

Burton AJ, Pregitzer KS (2003) Field measurements of root respiration indicate little to no seasonal temperature acclimation for sugar maple and red pine. Tree Physiology 23, 273–280.
PubMed |
open url image1

Burton AJ, Pregitzer KS, Zogg GP, Zak DR (1998) Drought reduces root respiration in sugar maple forests. Ecological Applications 8, 771–778. open url image1

Burton AJ, Pregitzer KS, Ruess RW, Hendrik RL, Allen MF (2002) Root respiration in North American forests, effects of nitrogen concentration and temperature across biomes. Oecologia 131, 559–568.
CrossRef | open url image1

Carey EV, DeLucia EH, Ball JT (1996) Stem maintenance and construction respiration in Pinus ponderosa grown in different concentrations of atmospheric CO2. Tree Physiology 16, 125–130.
PubMed |
open url image1

Chabot BF, Billings WD (1972) Origins and ecology of the Sierran alpine flora and vegetation. Ecological Monographs 42, 163–199. open url image1

Clarkson, DT , Earnshaw, MJ , White, PJ ,  and  Cooper, HD (1988). Temperature dependent factors influencing nutrient uptake, an analysis of responses at different levels of organization. In ‘Plants and temperature’. pp. 281–309. (Company of Biologists: Cambridge)

Collier DE (1996) No difference in leaf respiration rates among temperate, subarctic, and arctic species grown under controlled conditions. Canadian Journal of Botany 74, 317–320. open url image1

Collier DE, Cummins WR (1990) The effects of low growth and measurement temperature on the respiratory properties of five temperate species. Annals of Botany 65, 533–538. open url image1

Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18, 388–397.
CrossRef | open url image1

Covey-Crump EM, Attwood RG, Atkin OK (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 and Environment 25, 1501–1513.
CrossRef | open url image1

Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187.
CrossRef | PubMed | open url image1

Cramer W, Bondeau A, Woodward FI, Prentice IC, Betts RA , et al. (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change, results from six dynamic global vegetation models. Global Change Biology 7, 357–373.
CrossRef | open url image1

Crawford RMM, Palin MA (1981) Root respiration and temperature limits to the north-south distribution of four perennial maritime plants. Flora 171, 338–354. open url image1

Criddle RS, Hopkin MS, McArthur ED, Hansen LD (1994) Plant distribution and the temperature coefficient of metabolism. Plant, Cell and Environment 17, 233–243. open url image1

Damesin C, Ceschina E, Le Goff N, Ottorini J, Dufrêne E (2002) Stem and branch respiration of beech, from tree measurements to estimations at the stand level. New Phytologist 153, 159–172.
CrossRef | open url image1

Dewar RC, Medlyn BE, McMurtrie RE (1999) Acclimation of the respiration / photosynthesis ratio to temperature, insights from a model. Global Change Biology 5, 615–622.
CrossRef | open url image1

Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, de Paepe R (2003) Leaf mitochondrial module whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signalling and diurnal regulation. The Plant Cell 15, 1212–1226.
CrossRef | PubMed | open url image1

Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR , et al. (1997) Maximum and minimum temperature trends for the globe. Science 277, 364–366.
CrossRef | open url image1

Edwards EJ, Benham DG, Marland LA, Fitter AH (2004) Root production is determined by radiation flux in a temperate grassland community. Global Change Biology 10, 209–227.
CrossRef |
open url image1

Edwards NT, Tschaplinski TJ, Norby RJ (2002) Stem respiration increases in CO2-enriched sweetgum trees. New Phytologist 155, 239–248.
CrossRef | open url image1

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
CrossRef | open url image1

Farrar JF, Williams ML (1991) The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant, Cell and Environment 4, 819–830. open url image1

Field CB (2001) Plant physiology of the ‘missing’ carbon sink. Plant Physiology 125, 25–28.
CrossRef | PubMed | open url image1

Fitter AH, Graves JD, Self GK, Brown TK, Bogie DS, Taylor K (1998) Root production, turnover and respiration under two grassland types along an altitudinal gradient — influence of temperature and solar radiation. Oecologia 114, 20–30.
CrossRef | open url image1

Forward, DF (1960). Effect of temperature on respiration. In ‘Encyclopedia of plant physiology. Vol. 12’. pp. 234–258. (Springer-Verlag: Berlin)

Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum 100, 241–254.
CrossRef | open url image1

Foyer CH, Noctor G (2000) Tansley Review NO 112. Oxygen processing in photosynthesis, regulation and signalling. New Phytologist 146, 359–388.
CrossRef | open url image1

Frantz JM, Cometti NN, Bugbee BRUC (2004) Night temperature has a minimal effect on respiration and growth in rapidly growing plants. Annals of Botany 94, 155–166.
CrossRef | PubMed | open url image1

Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
CrossRef | PubMed | open url image1

Gielen B, Scarascia-Mugnozza G, Ceulemans R (2003) Stem respiration of Populus species in the third year of free-air CO2 enrichment. Physiologia Plantarum 117, 500–507.
CrossRef | PubMed |
open url image1

Gifford RM (1995) Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature — long-term versus short-term distinctions for modelling. Global Change Biology 1, 385–396. open url image1

Gifford RM (2003) Plant respiration in productivity models, conceptualisation, representation and issues for global terrestrial carbon-cycle research. Functional Plant Biology 30, 171–186.
CrossRef | open url image1

Goldstein G, Drake DR, Melcher P, Giambelluca TW, Heraux J (1996) Photosynthetic gas exchange and temperature-induced damage in seedlings of the tropical alpine species Argyroxiphium sandwicense. Oecologia 106, 298–307.
CrossRef | open url image1

Gonzàlez-Meler MA, Ribas-Carbó M, Giles L, Siedow JN (1999) The effect of growth and measurement temperature on the activity of the alternative respiratory pathway. Plant Physiology 120, 765–772.
CrossRef | PubMed | open url image1

Gonzàlez-Meler MA, Taneva LINA, Trueman RJ (2004) Plant respiration and elevated atmospheric CO2 concentration: cellular responses and global significance. Annals of Botany 94, 647–656.
CrossRef | PubMed | open url image1

Griffin KL, Turnbull M, Murthy R (2002) Canopy position affects the temperature response of leaf respiration in Populus deltoides. New Phytologist 154, 609–619.
CrossRef | open url image1

Gunn S, Farrar JF (1999) Effects of a 4°C increase in temperature on partitioning of leaf area and dry mass, root respiration and carbohydrates. Functional Ecology 13, 12–20.
CrossRef | open url image1

Hamilton JG, Thomas RB, Delucia EH (2001) Direct and indirect effects of elevated CO2 on leaf respiration in a forest ecosystem. Plant, Cell and Environment 24, 975–982.
CrossRef | open url image1

Harley PC, Thomas RB, Reynolds J (1992) Modeling photosynthesis of cotton grown in elevated CO2. Plant, Cell and Environment 15, 271–282. open url image1

Higgins PD, Spomer GG (1976) Soil temperature effects on root respiration and the ecology of alpine and subalpine plants. Botanical Gazette 137, 110–120.
CrossRef | open url image1

Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta 1366, 235–255. open url image1

Holmgren P, Jarvis PG (1967) Carbon dioxide efflux from leaves in light and darkness. Physiologia Plantarum 20, 1045–1051. open url image1

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 Physiology 106, 983–990.
PubMed |
open url image1

Hurry VM, Tobiæson M, Krömer S, Gardeström P, Öquist G (1995) Mitochondria contribute to increased photosynthetic capacity of leaves of winter rye (Secale cereale L.) following cold-hardening. Plant, Cell and Environment 18, 69–76. open url image1

Hurry VM, Keerberg O, Pärnik T, Öquist G, Gardeström P (1996) Effect of cold hardening on the components of respiratory decarboxylation in the light and in the dark in leaves of winter rye. Plant Physiology 111, 713–719.
PubMed |
open url image1

Ivanova, TL , Semikhatova, OA , Judina, OS ,  and  Leina, GD (1989). The effect of temperature on the respiration of plants from different plant-geographic zones. In ‘Ecophysiological investigations of photosynthesis and respiration in plants’. pp. 140–166. (Nauka Publishing, Nauka: St Petersberg)

James, WO (1953). ‘Plant respiration.’ (Clarendon Press: Oxford)

Janouš D, Pokornyý R, Brossaud J, Marek MV (2000) Long-term effects of elevated CO2 on woody tissues respiration in Norway spruce studied in open-top chambers. Biologia Plantarum 43, 41–46.
CrossRef | open url image1

Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657.
CrossRef | PubMed | open url image1

Klikoff LG (1966) Temperature dependence of the oxidative rates of mitochondria in Danthonia intermedia, Penstemon davidsonii and Sitanion hystrix. Nature 212, 529–530. open url image1

Klikoff LG (1968) Temperature dependence of mitochondrial oxidative rates of several plant species of the Sierra Nevada. Botanical Gazette 129, 227–230.
CrossRef | open url image1

Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509–540.
CrossRef | PubMed | open url image1

Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymology 13, 1–56. open url image1

Kurimoto K, Day DA, Lambers H, Noguchi K (2004a) Effect of respiratory homeostasis on plant growth in cultivars of wheat and rice. Plant, Cell and Environment 27, 853–862.
CrossRef | open url image1

Kurimoto K, Millar AH, Lambers H, Day DA, Noguchi K (2004b) Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant and Cell Physiology 45, 1015–1022.
CrossRef | PubMed | open url image1

Körner, C (1999). ‘Alpine plant life. Functional plant ecology of high mountain ecosystems.’ (Springer-Verlag: Berlin)

Körner, C ,  and  Larcher, W (1988). Plant life in cold environments. In ‘Plants and temperature. Symposium of the Society of Experimental Biologists. Vol. 42’. pp. 25–57. (The Company of Biologists Limited: Cambridge)

Krömer S (1995) Respiration during photosynthesis. Annual Review of Plant Physiology and Molecular Biology 46, 45–70.
CrossRef | open url image1

Laisk, AK (1977). ‘Kinetics of photosynthesis and photorespiration in C-plants.’ (Nauka: Moscow)

Larigauderie A, Körner C (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Annals of Botany 76, 245–252.
CrossRef | open url image1

Loreto F, Delfine S, DiMarco G (1999) Estimation of photorespiratory carbon dioxide recycling during photosynthesis. Australian Journal of Plant Physiology 26, 733–736. open url image1

Loreto F, Velikova V, Di Marco G (2001) Respiration in the light measured by (CO2)-C12 emission in (CO2)-C13 atmosphere in maize leaves. Australian Journal of Plant Physiology 28, 1103–1108. open url image1

Loveys BR, Scheurwater I, Pons TL, Fitter AH, Atkin OK (2002) Growth temperature influences the underling components of relative growth rate, an investigation using inherently fast- and slow-growing plant species. Plant, Cell and Environment 25, 975–987.
CrossRef | open url image1

Loveys BR, Atkinson LJ, Sherlock DJ, Roberts RL, Fitter AH, Atkin OK (2003) Thermal acclimation of leaf and root respiration, an investigation comparing inherently fast- and slow-growing plant species. Global Change Biology 9, 895–910.
CrossRef | open url image1

Luo YQ, Wan SQ, Hui DF, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413, 622–625.
CrossRef | PubMed | open url image1

Maxwell DP, Wang Y, Mcintosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences USA 96, 8271–8276.
CrossRef | open url image1

McCashin BG, Cossins EA, Canvin DT (1988) Dark respiration during photosynthesis in wheat leaf slices. Plant Physiology 87, 155–161. open url image1

Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiology 133, 443–447.
CrossRef | PubMed | open url image1

Miroslavov EA, Kravkina IM (1991) Comparative analysis of chloroplasts and mitochondria in leaf chlorenchyma from mountain plants grown at different altitudes. Annals of Botany 68, 195–200. open url image1

Møller IM (2001) Plant mitochondria and oxidative stress, electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561–591.
CrossRef | PubMed | open url image1

Mooney HA, Billings WD (1965) Effects of altitude on carbohydrate content of mountain plants. Ecology 46, 750–751. open url image1

Nantes IL, Fagian MM, Catisti R, Arruda P, Maia IG, Vercesi AE (1999) Low temperature and aging-promoted expression of PUMP in potato tuber mitochondria. FEBS Letters 457, 103–106.
CrossRef | PubMed | open url image1

Noctor G, Dutilleul C, De Paepe R, Foyer CH (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon / nitrogen metabolism. Journal of Experimental Botany 55, 49–57.
CrossRef | PubMed |
open url image1

Oleksyn J, Zytkowiak R, Reich PB, Tjoelker MG, Karolewski P (2000) Ontogenetic patterns of leaf CO2 exchange, morphology and chemistry in Betula pendula trees. Trees 14, 271–281.
CrossRef | open url image1

Padmasree K, Padmavathi L, Raghavendra AS (2002) Essentiality of mitochondrial oxidative metabolism for photosynthesis, optimization of carbon assimilation and protection against photoinhibition. Critical Reviews in Biochemistry and Molecular Biology 37, 71–119.
CrossRef | PubMed | open url image1

Paembonan SA, Hagihara A, Hozumi K (1991) Long-term measurement of CO2 release from the above-ground parts of a hinoki forest tree in relation to air temperature. Tree Physiology 8, 399–405. open url image1

Pärnik T, Keerberg O (1995) Decarboxylation of primary and end products of photosynthesis at different oxygen concentrations. Journal of Experimental Botany 46, 1439–1447. open url image1

Pisek, A , Larcher, W , Vegis, A ,  and  Napp-Zinn, K (1973). The normal temperature range. In ‘Temperature and life’. pp. 102–194. (Springer-Verlag: Berlin)

Popov VN, Simonian RA, Skulachev VP, Starkov AA (1997) Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Letters 415, 87–90.
CrossRef | PubMed | open url image1

Pons TL, Welschen RAM (2003) Midday depression of net photosynthesis in the tropical rainforest tree Eperua grandiflora: contributions of stomatal and internal conductances, respiration and Rubisco functioning. Tree Physiology 23, 937–947.
PubMed |
open url image1

Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology 94, 621–627. open url image1

Prasad TK, Anderson MD, Stewart CR (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology 105, 619–627.
PubMed |
open url image1

Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL (1997) Root architecture, carbon and nitrogen in four temperate forest species. Oecologia 111, 302–308.
CrossRef | open url image1

Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiology 18, 665–670.
PubMed |
open url image1

Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiologia Plantarum 100, 165–170.
CrossRef | open url image1

Purvis AC, Shewfelt RL (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiologia Plantarum 88, 712–718.
CrossRef | open url image1

Raghavendra AS, Padmasree K, Saradadevi K (1994) Interdependence of photosynthesis and respiration in plant cells — interactions between chloroplasts and mitochondria. Plant Science 97, 1–14.
CrossRef | open url image1

Raich JW, Schlesinger WH (1992) The global carbon-dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus Series–Chem Phys Meteor 44, 81–99. open url image1

Reichstein M, Tenhunen JD, Roupsard O, Ourcival J-M, Rambal S, Dore S, Valentini R (2002) Ecosystem respiration in two Mediterranean evergreen Holm Oak forests, drought effects and decomposition dynamics. Functional Ecology 16, 27–39.
CrossRef | open url image1

Ribas-Carbó M, Aroca R, Gonzàlez-Meler MA, Irigoyen JJ, Sanchezdiaz M (2000) The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiology 122, 199–204.
CrossRef | PubMed | open url image1

Rook DA (1969) The influence of growing temperature on photosynthesis and respiration of Pinus radiata seedlings. New Zealand Journal of Botany 7, 43–55. open url image1

Ryan MG (1991) Effects of climate change on plant respiration. Ecological Applications 1, 157–167. open url image1

Ryan MG, Hubbard RM, Pongracic S, Raison RJ, McMurtrie RE (1996) Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status. Tree Physiology 16, 333–343.
PubMed |
open url image1

Saradadevi K, Raghavendra AS (1992) Dark respiration protects photosynthesis against photoinhibition in mesophyll protoplasts of pea (Pisum sativum). Plant Physiology 99, 1232–1237. open url image1

Schimel DS, Emanuel W, Rizzo B, Smith T, Woodward FI , et al. (1997) Continental scale variability in ecosystem processes, models, data and the role of disturbance. Ecological Monographs 67, 251–271. open url image1

Semikhatova, OA , Gerasimenko, TV ,  and  Ivanova, TI (1992). Photosynthesis, respiration, and growth of plants in the Soviet Arctic. In ‘Arctic ecosystems in a changing climate’. pp. 169–192. (Academic Press: San Diego)

Shapiro JB, Griffin KL, Lewis JD, Tissue DT (2004) Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytologist 162, 377–386.
CrossRef | open url image1

Sheen J (1994) Feedback control of gene expression. Photosynthesis Research 39, 427–438.
CrossRef | open url image1

Shyam R, Raghavendra AS, Sane PV (1993) Role of dark respiration in photoinhibition of photosynthesis and its reactivation in the Cyanobacterium anacystis-nidulans. Physiologia Plantarum 88, 446–452.
CrossRef | open url image1

Smakman G, Hofstra RJJ (1982) Energy metabolism of Plantago lanceolata, as affected by change in root temperature. Physiologia Plantarum 56, 33–37. open url image1

Sowell JB, Spomer GG (1986) Ecotypic variation in root respiration rate among elevational populations of Abies lasiocarpa and Picea engelmannii. Oecologia 68, 375–379.
CrossRef |
open url image1

Stockfors J, Linder S (1998) The effect of nutrition on the seasonal course of needle respiration in Norway spruce stands. Trees 12, 130–138.
CrossRef | open url image1

Strand A, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. The Plant Journal 12, 605–614.
CrossRef | PubMed | open url image1

Strand A, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant, Cell and Environment 26, 523–535.
CrossRef |
open url image1

Stitt M, Hurry VM (2002) A plant for all seasons: alteration in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Current Opinion in Plant Biology 5, 199–206.
CrossRef | PubMed | open url image1

Talts P, Parnik T, Gardestrom P, Keerberg O (2004) Respiratory acclimation in Arabidopsis thaliana leaves at low temperature. Journal of Plant Physiology 161, 573–579.
PubMed |
open url image1

Tjoelker MG, Oleksyn J, Reich PB (1999a) Acclimation of respiration to temperature and CO2 in seedlings of boreal tree species in relation to plant size and relative growth rate. Global Change Biology 5, 679–691.
CrossRef | open url image1

Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q10. Global Change Biology 7, 223–230.
CrossRef | open url image1

Tjoelker MG, Reich PB, Oleksyn J (1999b) Changes in leaf nitrogen and carbohydrates underlie temperature and CO2 acclimation of dark respiration in five boreal tree species. Plant, Cell and Environment 22, 767–778.
CrossRef | open url image1

Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Griffin KL (2001) Responses of leaf respiration to temperature and leaf characteristics in three deciduous tree species vary with site water availability. Tree Physiology 21, 571–578.
PubMed |
open url image1

Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Griffin KL (2003) Scaling foliar respiration in two contrasting forest canopies. Functional Ecology 17, 101–114.
CrossRef | open url image1

Vanlerberghe GC, McIntosh L (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiology 100, 115–119. open url image1

Villar R, Held AA, Merino J (1995) Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiology 107, 421–427.
PubMed |
open url image1

Wagner AM (1995) A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Letters 368, 339–342.
CrossRef | PubMed | open url image1

Wager HG (1941) On the respiration and carbon assimilation rates of some arctic plants as related to temperature. New Phytologist 40, 1–19. open url image1

Warren Wilson J (1966) An analysis of plant growth and its control in Arctic environments. Annals of Botany 30, 383–402. open url image1

Weger HG, Guy RD (1991) Cytochrome and alternative pathway respiration in white spruce (Picea glauca) roots. Effects of growth and measurement temperature. Physiologia Plantarum 83, 675–681.
CrossRef | open url image1

White A, Cannell MGR, Friend AD (2000) The high-latitude terrestrial carbon sink, a model analysis. Global Change Biology 6, 227–245.
CrossRef | open url image1

Will R (2000) Effect of different daytime and night-time temperature regimes on the foliar respiration of Pinus taeda: predicting the effect of variable temperature on acclimation. Journal of Experimental Botany 51, 1733–1739.
CrossRef | PubMed | open url image1

Wythers KR, Reich PB, Tjoelker MG, Bolstad PB (2005) Foliar respiration acclimation to temperature and temperature variable Q10 alter ecosystem carbon balance. Global Change Biology (In press) , open url image1

Xiong FS, Mueller EC, Day TA (2000) Photosynthetic and respiratory acclimation and growth response of antarctic vascular plants to contrasting temperature regimes. American Journal of Botany 87, 700–710.
PubMed |
open url image1

Zha TS, Ryyppö A, Wang KY, Kellomäki S (2001) Effects of elevated carbon dioxide concentration and temperature on needle growth, respiration and carbohydrate status in field-grown Scots pines during the needle expansion period. Tree Physiology 21, 1279–1287.
PubMed |
open url image1

Zha TS, Wang KY, Ryyppö A, Kellomäki S (2002) Impact of needle age on the response of respiration in Scots pine to long-term elevation of carbon dioxide concentration and temperature. Tree Physiology 22, 1241–1248.
PubMed |
open url image1

Zha TS, Kellomäki S, Wang KY (2003) Seasonal variation in respiration of 1-year-old shoots of Scots pine exposed to elevated carbon dioxide and temperature for 4 years. Annals of Botany 92, 89–96.
CrossRef | PubMed | open url image1

Zha T, Kellomäki S, Wang KY, Ryyppö A, Niinisto S (2004) Seasonal and annual stem respiration of Scots Pine trees under boreal conditions. Annals of Botany 94, 889–896.
CrossRef | PubMed | open url image1

Zha TS, Kellomäki S, Wang KY, Ryyppö A (2005) Respiratory responses of Scots pine stems to 5 years of exposure to elevated CO2 concentration and temperature. Tree Physiology 25, 49–56.
PubMed |
open url image1

Zimmerman RC, Smith RD, Alberte RS (1989) Thermal acclimation and whole-plant carbon balance in Zostera marina L (Eelgrass). Journal of Experimental Marine Biology and Ecology 130, 93–109.
CrossRef | open url image1

Ziska LH, Bunce JA (1998) The influence of increasing growth temperature and CO2 concentration on the ratio of respiration to photosynthesis in soybean seedlings. Global Change Biology 4, 637–643.
CrossRef | open url image1

Zogg GP, Zak DR, Burton AJ, Pregitzer KS (1996) Fine root respiration in northern hardwood forests in relation to temperature and nitrogen availability. Tree Physiology 16, 719–725.
PubMed |
open url image1

Xu M, Debiase TA, Qi Y, Goldstein A, Liu Z (2001) Ecosystem respiration in a young ponderosa pine plantation in the Sierra Nevada Mountains, California. Tree Physiology 21, 309–318.
PubMed |
open url image1







Full Text PDF (294 KB) Export Citation Cited By (213)