Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Acclimation of leaf dark respiration to nocturnal and diurnal warming in a semiarid temperate steppe

Yonggang Chi A B , Ming Xu A C E , Ruichang Shen A and Shiqiang Wan D
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China.

B State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.

C Department of Ecology, Evolution and Natural Resources, Center for Remote Sensing and Spatial Analysis, Rutgers University, NJ 08901, USA.

D Key Laboratory of Plant Stress Biology, College of Life Sciences, Henan University, Henan 475004, China.

E Corresponding author. Email: mingxu@igsnrr.ac.cn

Functional Plant Biology 40(11) 1159-1167 https://doi.org/10.1071/FP12369
Submitted: 9 December 2012  Accepted: 13 May 2013   Published: 19 June 2013

Abstract

A better understanding of thermal acclimation of leaf dark respiration in response to nocturnal and diurnal warming could help accurately predict the changes in carbon exchange of terrestrial ecosystems under global warming, especially under the asymmetric warming. A field manipulative experiment was established with control, nocturnal warming (1800–0600 hours), diurnal warming (0600–1800 hours), and diel warming (24 h) under naturally fluctuating conditions in a semiarid temperate steppe in northern China in April 2006. Temperature response curves of in situ leaf dark respiration for Stipa krylovii Roshev. were measured at night (Rn) and after 30 min of darkness imposed in the daytime (Rd). Leaf nonstructural carbohydrates were determined before sunrise and at sunset. Results showed that Rn could acclimate to nocturnal warming and diurnal warming, but Rd could not. The decreases in Q10 (temperature sensitivity) of Rn under nocturnal-warming and diurnal warming regimes might be attributed to greater depletion of total nonstructural carbohydrates (TNC). The real-time and intertwined metabolic interactions between chloroplastic and mitochondrial metabolism in the daytime could affect the impacts of warming on metabolite pools and the distinct response of Rn and Rd to warming. Projection on climate change–carbon feedback under climate warming must account for thermal acclimation of leaf dark respiration separately by Rn and Rd.

Additional keywords: carbon, climate warming, grassland, nonstructural carbohydrates, Q10, temperature.


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.
A generalized, lumped-parameter model of photosynthesis, evapotranspiration and net primary production in temperate and boreal forest ecosystems.Crossref | GoogleScholarGoogle Scholar |

Alward RD, Detling JK, Milchunas DG (1999) Grassland vegetation changes and nocturnal global warming Science 283, 229–231.
Grassland vegetation changes and nocturnal global warmingCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtlelug%3D%3D&md5=ab25ee9328fbcafea3659edc84597835CAS | 9880257PubMed |

Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
Thermal acclimation and the dynamic response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1CjtLk%3D&md5=9f04e0b89109b04172cb710701d9678dCAS | 12878019PubMed |

Atkin OK, Holly C, Ball MC (2000) 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 & Environment 23, 15–26.
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.Crossref | GoogleScholarGoogle Scholar |

Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology 32, 87–105.
The hot and the cold: unravelling the variable response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar |

Bai W, Xia J, Wan S, Zhang W, Li L (2012) Day and night warming have different effect on root lifespan. Biogeosciences 9, 375–384.
Day and night warming have different effect on root lifespan.Crossref | GoogleScholarGoogle Scholar |

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.
Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra.Crossref | GoogleScholarGoogle Scholar |

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.
The respiratory energy requirements involved in nocturnal carbohydrate export from starch-storing mature source leaves and their contribution to leaf dark respiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovV2mt70%3D&md5=87a83c2bf294f96ea8ec22016220f227CAS |

Bruhn D, Egerton JJG, Loveys BR, Ball MC (2007) Evergreen leaf respiration acclimates to long-term nocturnal warming under field conditions. Global Change Biology 13, 1216–1223.
Evergreen leaf respiration acclimates to long-term nocturnal warming under field conditions.Crossref | GoogleScholarGoogle Scholar |

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 Phytologist 176, 375–389.
Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Cnt7rL&md5=a940e9a9762b2d444ec770e1f7afd7a2CAS | 17692077PubMed |

Christensen L, Coughenour MB, Ellis JE, Chen Z (2004) Vulnerability of the Asian typical steppe to grazing and climate change. Climatic Change 63, 351–368.
Vulnerability of the Asian typical steppe to grazing and climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsl2ns7g%3D&md5=943a25fb78ce11cc5c3f34509d36f8bbCAS |

Cramer W, Bondeau A, Woodward FI, Prentice IC, Betts RA, Brovkin V, Cox PM, Fisher V, Foley JA, Friend AD, Kucharik C, Lomas MR, Ramankutty N, Sitch S, Smith B, White A, Young-Molling C (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.
Global response of terrestrial ecosystem structure and function to CO2 and climate change, results from six dynamic global vegetation models.Crossref | GoogleScholarGoogle Scholar |

Crous KY, Zaragoza-Castells J, Löw M, Ellsworth DS, Tissue DT, Tjoelker MG, Barton CVM, Gimeno TE, Atkin OK (2011) Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: impacts of elevated atmospheric CO2 conditions and summer drought. Global Change Biology 17, 1560–1576.
Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: impacts of elevated atmospheric CO2 conditions and summer drought.Crossref | GoogleScholarGoogle Scholar |

Dillaway DN, Kruger EL (2011) Leaf respiratory acclimation to climate: comparisons among boreal and temperate tree species along a latitudinal transect. Tree Physiology 31, 1114–1127.
Leaf respiratory acclimation to climate: comparisons among boreal and temperate tree species along a latitudinal transect.Crossref | GoogleScholarGoogle Scholar | 21990024PubMed |

Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE, Salinger MJ, Razuvayev V, Plummer N, Jamason P, Folland CK (1997) Maximum and minimum temperature trends for the globe Science 277, 364–367.
Maximum and minimum temperature trends for the globeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvVels78%3D&md5=14614c227e96dc856f36f56f7cd98ee6CAS |

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=b0417117f3598df013ab17a3da1f67a8CAS |

Florez-Sarasa I, Araújo WL, Wallström AV, Rasmusson AG, Fernie AR, Ribas-Carbo M (2012) Light-responsive metabolite and transcript levels are maintained following a dark-adaptation period in leaves of Arabidopsis thaliana. New Phytologist 195, 136–148.
Light-responsive metabolite and transcript levels are maintained following a dark-adaptation period in leaves of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSgtr7M&md5=44fe4b4b445c70d4c10b145a479e7b89CAS | 22548389PubMed |

Griffin KL, Turnbull R, Murthy R, Lin G, Adams J, Farnsworth B, Mahato T, Bazins 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.
Leaf respiration is differentially affected by leaf vs. stand-level night-time warming.Crossref | GoogleScholarGoogle Scholar |

Hendrix DL (1993) Rapid extraction and analysis of nonstructural carbohydrates in plant tissues. Crop Science 33, 1306–1311.
Rapid extraction and analysis of nonstructural carbohydrates in plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXjtFymur8%3D&md5=38d183bc1a78bbaa5e811f4535e71c2cCAS |

Hurry V, Igamberdiev AU, Keerberg O, Pärnik T, Atkin OK, Zaragoza-Castells J, Gardeström P (2005) Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In ‘Plant respiration: from cell to ecosystem. Vol. 18. Advances in photosynthesis and respiration series’. (Eds H Lambers, M Ribas-Carbo) pp. 43–61. (Springer: Dordrecht, The Netherlands)

Krömer S, Malmberg G, Gardeström P (1993) Mitochondrial contribution to photosynthetic metabolism – a study with barley (Hordeum vulgare L.) leaf protoplasts at different light intensities and CO2 concentrations. Plant Physiology 102, 947–955.

Lee TD, Reich PB, Bolstad PV (2005) Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species. Functional Ecology 19, 640–647.
Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species.Crossref | GoogleScholarGoogle Scholar |

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. Global Change Biology 16, 288–302.
Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not.Crossref | GoogleScholarGoogle Scholar |

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.
Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWnsbY%3D&md5=021e9eace011f80584080909b8073284CAS | 12027265PubMed |

Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101, 9971–9975.
Rice yields decline with higher night temperature from global warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOiu78%3D&md5=267e06d10a6fdb062c5051378222445aCAS | 15226500PubMed |

Reichstein M, Ciais P, Papale D, Valentini R, Running S, Viovy N, Cramer W, Granier A, Ogée J, Allard V, Aubinet M, Bernhofer C, Buchmann N, Carrara A, Grünwald T, Heimann M, Heinesch B, Knohl A, Kutsch W, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Pilegaard K, Pumpanen J, Rambal S, Schaphoff S, Seufert G, Soussana JF, Sanz MJ, Vesala T, Zhao M (2007) Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Global Change Biology 13, 634–651.
Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis.Crossref | GoogleScholarGoogle Scholar |

Rodríguez-Calcerrada J, Jaeger C, Limousin JM, Ourcival JM, Joffre R, Rambal S (2011) Leaf CO2 efflux is attenuated by acclimation of respiration to heat and drought in a Mediterranean tree. Functional Ecology 25, 983–995.
Leaf CO2 efflux is attenuated by acclimation of respiration to heat and drought in a Mediterranean tree.Crossref | GoogleScholarGoogle Scholar |

Rodríguez-Calcerrada J, Limousin JM, Martin-StPaul NK, Jaeger C, Rambal S (2012) Gas exchange and leaf aging in an evergreen oak: causes and consequences for leaf carbon balance and canopy respiration. Tree Physiology 32, 464–477.
Gas exchange and leaf aging in an evergreen oak: causes and consequences for leaf carbon balance and canopy respiration.Crossref | GoogleScholarGoogle Scholar | 22491489PubMed |

Ryan GR (1991) Effects of climate change on plant respiration. Ecological Applications 1, 157–167.
Effects of climate change on plant respiration.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.
Continental scale variability in ecosystem processes, models, data and the role of disturbance.Crossref | GoogleScholarGoogle Scholar |

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=dd89a3df7229523795151fc64a2761feCAS |

Teskey RO, Will RE (1999) Acclimation of loblolly pine (Pinus taeda) seedlings to high temperatures. Tree Physiology 19, 519–525.
Acclimation of loblolly pine (Pinus taeda) seedlings to high temperatures.Crossref | GoogleScholarGoogle Scholar | 12651542PubMed |

Thornton PE, Law BE, Gholz HL, Clark KL, Falge E, Ellsworth DS, Goldstein AH, Monsong RK, Hollinger D, Falk M, Chen J, Sparks JP (2002) Modeling and measuring the effects of disturbance history and climate on carbon and water budgets in evergreen needleleaf forests. Agricultural and Forest Meteorology 113, 185–222.
Modeling and measuring the effects of disturbance history and climate on carbon and water budgets in evergreen needleleaf forests.Crossref | GoogleScholarGoogle Scholar |

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

Tjoelker MG, Oleksyn J, Reich PB, Zytkowiak R (2008) Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations. Global Change Biology 14, 782–797.
Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations.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.
Responses of leaf respiration to temperature and leaf characteristics in three deciduous tree species vary with site water availability.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fht1Gquw%3D%3D&md5=53e81f8bbfffd893f5ac98ac1f6cf297CAS | 11390301PubMed |

Turnbull MH, Tissue DT, Murthy R, Wang X, Sparrow AD, Griffin KL (2004) Nocturnal warming increases photosynthesis at elevated CO2 partial pressure in Populus deltoids. New Phytologist 161, 819–826.
Nocturnal warming increases photosynthesis at elevated CO2 partial pressure in Populus deltoids.Crossref | GoogleScholarGoogle Scholar |

Urbanczyk-Wochniak E, Baxter C, Kolbe A, Kopka J, Sweetlove LJ, Fernie AR (2005) Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves. Planta 221, 891–903.
Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXos1emtLw%3D&md5=fe9933198ad5e67ff26b93168ebb04dbCAS | 15744496PubMed |

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtFyjug%3D%3D&md5=3387f565dfaf023128aa42635b34a338CAS |

Wan S, Xia J, Liu W, Niu S (2009) Photosynthetic overcompensation under nocturnal warming enhances grassland carbon sequestration. Ecology 90, 2700–2710.
Photosynthetic overcompensation under nocturnal warming enhances grassland carbon sequestration.Crossref | GoogleScholarGoogle Scholar | 19886480PubMed |

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

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.
Effect of different daytime and night-time temperature regimes on the foliar respiration of Pinus taeda: predicting the effect of variable temperature on acclimation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVWis7s%3D&md5=efd91bccef4d02ce89cd3f4661ff6145CAS | 11053463PubMed |

Xia J, Han Y, Zhang Z, Zhang Z, Wan S (2009) Effects of diurnal warming on soil respiration are not equal to the summed effects of day and night warming in a temperate steppe. Biogeosciences 6, 1361–1370.
Effects of diurnal warming on soil respiration are not equal to the summed effects of day and night warming in a temperate steppe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKjtLnJ&md5=bfff6f46e335f97d718b6307f1e3f594CAS |

Xu M, Qi Y (2001) Spatial and seasonal variations of Q 10 determined by soil respiration measurements at a Sierra Nevadan forest. Global Biogeochemical Cycles 15, 687–696.
Spatial and seasonal variations of Q 10 determined by soil respiration measurements at a Sierra Nevadan forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslSks78%3D&md5=926d80b5498c7d742983291d187329e0CAS |