Transient shade and drought have divergent impacts on the temperature sensitivity of dark respiration in leaves of Geum urbanum
Martijn Slot A C , Joana Zaragoza-Castells A and Owen K. Atkin B DA Department of Biology, University of York, PO Box 373, York YO10 5YW, UK.
B Functional Ecology Group, Research School of Biological Sciences, Australian National University, Canberra, ACT 0200, Australia.
C Present address: Department of Botany, University of Florida, Gainesville, FL 32611, USA.
D Corresponding author. Email: owen.atkin@anu.edu.au
Functional Plant Biology 35(11) 1135-1146 https://doi.org/10.1071/FP08113
Submitted: 7 April 2008 Accepted: 1 August 2008 Published: 28 November 2008
Abstract
The respiratory response of plants to temperature is a critical biotic feedback in the study of global climate change. Few studies, however, have investigated the effects of environmental stresses on the short-term temperature response of dark respiration (Rdark) at the leaf level. We investigated the effect of shade and transient drought on the temperature sensitivity (Q10; the proportional increase in respiration per 10°C increase in temperature) of Rdark of Geum urbanum L. in controlled experiments. Shade effects were most pronounced following sustained, near-darkness, when rates of leaf Rdark at a set measuring temperature (25°C) and the Q10 of Rdark were both reduced. By contrast, rates of leaf Rdark and the Q10 of Rdark both increased in response to the onset of severe water stress. Water stress was associated with a rapid (but reversible) decline in rates of light-saturated photosynthesis (Psat), stomatal closure (gs) and progressive wilting. Re-watering resulted in a rapid recovery of Psat, gs and a decline in the Q10 of Rdark (due to larger proportional reductions in the rate of Rdark measured at 25°C compared with those measured at 14°C). The concentration of soluble sugars in leaves did not decline during drought (5–7 day cycles) or shading, but during drought the starch concentration dropped, suggesting starch to sugar conversion helped to maintain homeostatic concentrations of soluble sugars. Thus, the drought and shade induced changes in Rdark were unlikely to be due to stress-induced changes in substrate supply. Collectively, the data highlight the dynamic responses of respiratory Q10 values to changes in water supply and sustained reductions in growth irradiance. If widespread, such changes in the Q10 of leaf respiration could have important implications for predicted rates of ecosystem carbon exchange in the future, particularly in areas that experience more frequent droughts.
Additional keywords: light, Q10, photosynthesis, water stress.
Acknowledgements
This study was supported by a Natural Environment Research Council (NERC) studentship (NERC/S/I/2003/11431; MS) a NUFFIC grant (TP 03/023; MS) from the Netherlands organisation for international cooperation in higher education and a grant from the NERC in the UK (NER/A/S/2001/01186; OKA). We thank David Sherlock for his expert technical assistance.
Armstrong AF,
Logan DC,
Tobin AK,
O’Toole P, Atkin OK
(2006) Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant, Cell & Environment 29, 940–949.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Armstrong AF,
Wardlaw KD, Atkin OK
(2007) Assessing the relationship between respiratory acclimation to the cold and photosystem II redox poise in Arabidopsis thaliana. Plant, Cell & Environment 30, 1513–1522.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Armstrong AF,
Badger MR,
Day DA,
Barthet M,
Smith P,
Whelan J,
Millar AH, Atkin OK
(2008) Dynamic changes in the mitochondrial electron transport chain underpinning thermal acclimation of leaf respiration. Plant, Cell & Environment 31, 1156–1169.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Atkin OK, Macherel D
(2009) Invited Review: The crucial role of plant mitochondrial in orchestrating drought tolerance. Annals of Botany in press ,
Atkin OK, Tjoelker MG
(2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Atkin OK,
Evans J, Siebke K
(1998) Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Australian Journal of Plant Physiology 25, 437–443.
Atkin OK,
Edwards EJ, Loveys BR
(2000) Response of root respiration to changes in temperature and its relevance to global warming. The New Phytologist 147, 141–154.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Atkin OK,
Zhang Q, 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 | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Atkin OK,
Atkinson LJ,
Fisher R,
Campbell CD,
Zaragoza-Castells J,
Woodward FI,
Pitchford J, Hurry V
(2008) Using temperature-dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate-vegetation model. Global Change Biology in press ,
Azcón-Bieto J, Osmond CB
(1983) Relationship between photosynthesis and respiration. The effect of carbohydrate status on the rate of CO2 production by respiration in darkened and illuminated wheat leaves. Plant Physiology 71, 574–581.
| PubMed |
Azcón-Bieto J,
Gonzalez-Meler MA,
Doherty W, Drake BG
(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 |
Björkman O, Demmig B
(1987) Photon yield of O2 evolution and chlorophyll fluorescence at 77k among vascular plants of diverse origins. Planta 170, 489–504.
| Crossref | GoogleScholarGoogle Scholar |
Blackman GE, Wilson GL
(1951) Physiological and ecological studies in the analysis of plant environment VII. An analysis of the differential effects of light intensity on the net assimilation rate, leaf area ratio and relative growth rate of different species. Annals of Botany 15, 374–408.
Boardman NK
(1977) Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28, 355–377.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 |
Bouma TJ,
De Visser R,
Van Leeuwen PH,
De Kock MJ, Lambers H
(1995) The respiratory energy requirements involved in nocturnal carbohydrate export from starch-storing mature source leaves and their contribution to leaf dark respiration. Journal of Experimental Botany 46, 1185–1194.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Brix H
(1962) The effect of water stress on the rates of photosynthesis and respiration in tomato plants and loblolly pine seedlings. Physiologia Plantarum 15, 10–20.
| Crossref | GoogleScholarGoogle Scholar |
Callister AN, Adams MA
(2006) Water stress impacts on respiratory rate, efficiency and substrates, in growing and mature foliage of Eucalyptus spp. Planta 224, 680–691.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Canadell JG,
Le Quere C,
Raupach MR,
Field CB,
Buitenhuis ET,
Ciais P,
Conway TJ,
Gillett NP,
Houghton RA, Marland G
(2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences of the United States of America 104, 18866–18870.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cannell MGR, Thornley JHM
(2000) Modelling the components of plant respiration: Some guiding principles. Annals of Botany 85, 45–54.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Collier DE, Cummins WR
(1993) Sensitivity of the cytochrome and alternative pathways to osmotic stress in leaf-slices of Saxifraga-cernua I. Journal of Plant Physiology 141, 745–749.
|
CAS |
Cornic G,
Papageorgiou I, Louason G
(1987) Effects of a rapid and a slow drought cycle followed by rehydration on stomatal and non-stomatal components of leaf photosynthesis in Phaseolus vulgaris L. Journal of Plant Physiology 126, 309–318.
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 & Environment 25, 1501–1513.
| Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Engelbrecht BMJ,
Dalling JW,
Pearson TR,
Wolf RL,
Galvez DA,
Koehler T,
Tyree MT, Kursar TA
(2006) Short dry spells in the wet season increase mortality of tropical pioneer seedlings. Oecologia 148, 258–269.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Escalona JM,
Flexas J, Medrano H
(1999) Stomatal and non-stomatal limitations of photosynthesis under water stress in field-grown grapevines. Australian Journal of Plant Physiology 26, 421–433.
Field CB, Mooney HA
(1983) Leaf age and seasonal effect on light, water and nutrient use efficiency in a California shrub. Oecologia 56, 348–355.
| Crossref | GoogleScholarGoogle Scholar |
Flexas J, Medrano H
(2002a) Drought-inhibition of Photosynthesis in C3 Plants: Stomatal and Non-stomatal Limitations Revisited. Annals of Botany 89, 183–189.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Flexas J, Medrano H
(2002b) Energy dissipation in C3 plants under drought. Functional Plant Biology 29, 1209–1215.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Flexas J,
Bota J,
Galmés J,
Medrano H, Ribas-Carbó M
(2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Galmés J,
Ribas-Carbó M,
Medrano H, Flexas J
(2007) Response of leaf respiration to water stress in Mediterranean species with different growth forms. Journal of Arid Environments 68, 206–222.
| Crossref | GoogleScholarGoogle Scholar |
Genty B,
Briantais JM, Viera da Silva JB
(1987) Effects of drought on primary photosynthetic processes of cotton leaves. Plant Physiology 83, 360–364.
|
CAS |
PubMed |
Ghashghaie J,
Duranceau M,
Badeck FW,
Cornic G,
Adeline M-T, Deleens E
(2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant, Cell & Environment 24, 505–515.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 | GoogleScholarGoogle Scholar | PubMed |
Griffin KL,
Turnbull M,
Murthy R,
Lin GH,
Adams J,
Farnsworth B,
Mahato T,
Bazin G,
Potasnak M, Berry JA
(2002) Leaf respiration is differentially affected by leaf vs. stand- level night-time warming. Global Change Biology 8, 479–485.
| Crossref | GoogleScholarGoogle Scholar |
Hartley IP,
Armstrong AF,
Ineson P,
Barron-Gafford G,
Murthy R, Atkin OK
(2006) The dependence of respiration on photosynthetic substrate supply and temperature: integrating leaf, soil and ecosystem measurements. Global Change Biology 12, 1954–1968.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ito Y,
Saisho D,
Nakazono M,
Tsutsumi N, Hirai A
(1997) Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 203, 121–129.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Keech O,
Pesquet E,
Ahad A,
Askne A,
Nordvall D,
Vodnala SM,
Tuominen H,
Hurry V,
Dizengremel P, Gardestrom P
(2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant, Cell & Environment 30, 1523–1534.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
King AW,
Gunderson CA,
Post WM,
Weston DJ, Wullschleger SD
(2006) Plant respiration in a warmer world. Science 312, 536–537.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lawlor DW, Fock H
(1977) Water stress induced changes in the amounts of some photosynthetic assimilation products and respiratory metabolites of sunflower leaves. Journal of Experimental Botany 28, 329–337.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 | GoogleScholarGoogle Scholar |
Lusk CH, Reich PB
(2000) Relationships of leaf dark respiration with light environment and tissue nitrogen content in juveniles of 11 cold-temperate tree species. Oecologia 123, 318–329.
| Crossref | GoogleScholarGoogle Scholar |
McCree KJ,
Kallsen CE, Richardson SG
(1984) Carbon balance of sorghum plants during osmotic adjustment to water stress. Plant Physiology 76, 898–902.
|
CAS |
PubMed |
Melillo JM
(1999) Warm, warm on the range. Science 283, 183–184.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Noguchi K, Terashima I
(1997) Different regulation of leaf respiration between Spinacia oleracea, a sun species, and Alocasia odora, a shade species. Physiologia Plantarum 101, 1–7.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Noguchi K,
Nakajima N, Terashima I
(2001) Acclimation of leaf respiratory properties in Alocasia odora following reciprocal transfers of plants between high- and low-light environments. Plant, Cell & Environment 24, 831–839.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Noguchi K,
Taylor NL,
Millar AH,
Lambers H, Day DA
(2005) Response of mitochondria to light intensity in the leaves of sun and shade species. Plant, Cell & Environment 28, 760–771.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ribas-Carbó M,
Taylor NL,
Giles L,
Busquets S,
Finnegan PM,
Day DA,
Lambers H,
Medrano H,
Berry JA, Flexas J
(2005) Effects of water stress on respiration in soybean (Glycine max. L.) leaves. Plant Physiology 139, 466–473.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ryan MG
(1991) Effects of climate change on plant respiration. Ecological Applications 1, 157–167.
| Crossref | GoogleScholarGoogle Scholar |
Schimel DS,
Participants VEMAP, Braswell BH
(1997) Continental scale variability in ecosystem processes: models, data, and the role of disturbance. Ecological Monographs 67, 251–271.
Sims DA, Pearcy RW
(1989) Photosynthetic characteristics of a tropical forest understory herb, Alocasia macrorrhiza, and a related crop species, Colocasia esculenta grown in contrasting light environments. Oecologia 79, 53–59.
| Crossref | GoogleScholarGoogle Scholar |
Sims DA, Pearcy RW
(1991) Photosynthesis and respiration in Alocasia macrorrhiza following transfers to high and low light. Oecologia 86, 447–453.
| Crossref | GoogleScholarGoogle Scholar |
Sims DA, Pearcy RW
(1994) Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance.I. Carbon balance and allocation at different daily photon flux densities. Plant, Cell & Environment 17, 881–887.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Taylor K
(1997) Biological Flora Of The British Isles. Geum urbanum L. Journal of Ecology 85, 705–720.
| Crossref | GoogleScholarGoogle Scholar |
Tezara W,
Mitchell VJ,
Driscoll SD, Lawlor DW
(1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 | GoogleScholarGoogle Scholar |
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.
|
CAS |
PubMed |
Turnbull MH,
Murthy R, Griffin KL
(2002) The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides. Plant, Cell & Environment 25, 1729–1737.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 | GoogleScholarGoogle Scholar |
Vanlerberghe GC, McIntosh L
(1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiology 100, 115–119.
|
CAS |
PubMed |
Watanabe CK,
Hachiya T,
Terashima I, Noguchi K
(2008) The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant, Cell & Environment 31, 1190–1202.
|
CAS |
Crossref |
PubMed |
Whitehead D,
Griffin KL,
Turnbull MH,
Tissue DT,
Engel VC,
Brown KJ,
Schuster WSF, Walcroft AS
(2004) Response of total night-time respiration to differences in total daily photosynthesis for leaves in a Quercus rubra L. canopy: implications for modelling canopy CO2 exchange. Global Change Biology 10, 925–938.
| Crossref | GoogleScholarGoogle Scholar |
Wright IJ,
Reich PB,
Atkin OK,
Lusk CH,
Tjoelker MG, Westoby M
(2006) Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites. The New Phytologist 169, 309–319.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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 11, 435–449.
| Crossref | GoogleScholarGoogle Scholar |
Yordanov I,
Velikova V, Tsonev T
(2000) Plant responses to drought and stress tolerance. Photosynthetica 38, 171–186.
|
CAS |
Crossref |
Zagdanska B
(1995) Respiratory energy demand for protein turnover and ion transport in wheat leaves upon water deficit. Physiologia Plantarum 95, 428–436.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zaragoza-Castells J,
Sánchez-Gómez D,
Valladares F,
Hurry V, Atkin OK
(2007) Does growth irradiance affect thermal acclimation and temperature-dependence of leaf respiration? Insights from a Mediterranean tree with long-lived leaves. Plant, Cell & Environment 30, 820–833.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zaragoza-Castells J,
Sánchez-Gómez D,
Hartley IP,
Matesanz S,
Valladares F,
Lloyd J, Atkin OK
(2008) Climate-dependent variations in leaf respiration in a dry-land, low productivity Mediterranean forest: the importance of acclimation in both high-light and shaded habitats. Functional Ecology 22, 172–184.