Whole-plant respiration and its temperature sensitivity during progressive carbon starvation
Martijn Slot A B D and Kaoru Kitajima A B C
+ Author Affiliations
- Author Affiliations
A Department of Biology, University of Florida, Gainesville, FL 32611, USA.
B Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Republic of Panama.
C Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.
D Corresponding author. Email: martijnslot78@gmail.com
Functional Plant Biology 42(6) 579-588 https://doi.org/10.1071/FP14329
Submitted: 28 November 2014 Accepted: 24 February 2015 Published: 23 March 2015
Abstract
Plant respiration plays a critical role in the C balance of plants. Respiration is highly temperature sensitive and small temperature-induced increases in whole-plant respiration could change the C balance of plants that operate close to their light-compensation points from positive to negative. Nonstructural carbohydrates are thought to play an important role in controlling respiration and its temperature sensitivity, but this role has not been studied at the whole-plant level. We measured respiration of whole Ardisia crenata Sims. seedlings and tested the hypothesis that darkness-induced C starvation would decrease the temperature sensitivity of whole-plant respiration. Compared with control plants, sugar and starch concentrations in darkened plants declined over time in all organs. Similarly, whole-plant respiration decreased. However, the temperature sensitivity of whole-plant respiration, expressed as the proportional increase in respiration per 10°C warming (Q10), increased with progressive C starvation. We hypothesise that growth respiration was suppressed in darkened plants and that whole-plant respiration represented maintenance respiration almost exclusively, which is more temperature sensitive. Alternatively, changes in the respiratory substrate during C starvation or increased involvement of alternative oxidase pathway respiration may explain the increase in Q10. Carbohydrates are important for respiration but it appears that even in C-starved A. crenata plants, carbohydrate availability does not limit respiration during short-term warming.
Additional keywords: Ardisia crenata, carbohydrate storage, global warming, plant carbon balance, respiratory substrate depletion.
References
Amthor JS (1984) The role of maintenance respiration in plant growth. Plant, Cell & Environment 7, 561–569.Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation – an alternative respiratory substrate for stressed plants. Trends in Plant Science 16, 489–498.
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=9f883caac5f5f6b40fa19682d0f826a1CAS | 12878019PubMed |
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.
| Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox poise of the quinone pool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVSruw%3D%3D&md5=a10fb0d2e0e28aa788acea1145dd4942CAS | 11788767PubMed |
Atkin OK, Bruhn D, Tjoelker MG (2005). Response of plant respiration to changes in temperature: mechanisms and consequences of variations in Q 10 values and acclimation. In ‘Plant respiration’. (Eds H Lambers, M Ribas-Carbo) pp. 95–135. (Springer: Dordrecht)
Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. The Journal of Cell Biology 133, 1251–1263.
| Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslKjsbY%3D&md5=5651c6192a97f1dce5a02a37da82b3c4CAS | 8682862PubMed |
Baber O, Slot M, Celis-Azofeifa G, Kitajima K (2014) Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species. Botany 92, 535–540.
| Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVegsrs%3D&md5=5be3a6f75b41499747bb9ecb6bd85886CAS |
Baltzer JL, Thomas SC (2007) Determinants of whole‐plant light requirements in Bornean rain forest tree saplings. Journal of Ecology 95, 1208–1221.
| Determinants of whole‐plant light requirements in Bornean rain forest tree saplings.Crossref | GoogleScholarGoogle Scholar |
Burton A, Pregitzer K, Ruess R, Hendrick R, Allen M (2002) Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes. Oecologia 131, 559–568.
| Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes.Crossref | GoogleScholarGoogle Scholar |
Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annual Review of Plant Biology 65, 667–687.
| Nonstructural carbon in woody plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWhtrjK&md5=f226e0b21caf4ba521a2dddb2383eb88CAS | 24274032PubMed |
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
| Calorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28XjvFynsg%3D%3D&md5=9ff167b1d78f5432978ff16c07bbe999CAS |
Frantz JM, Cometti NN, Bugbee B (2004) Night temperature has a minimal effect on respiration and growth in rapidly growing plants. Annals of Botany 94, 155–166.
| Night temperature has a minimal effect on respiration and growth in rapidly growing plants.Crossref | GoogleScholarGoogle Scholar | 15159217PubMed |
Gray GR, Maxwell DP, Villarimo AR, McIntosh L (2004) Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Reports 23, 497–503.
| Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVagtr%2FI&md5=ae69f9bd0f821c0c70b21a066f0601bfCAS | 15322810PubMed |
Griffin KL, Turnbull M, Murthy R (2002) Canopy position affects the temperature response of leaf respiration in Populus deltoides. New Phytologist 154, 609–619.
| Canopy position affects the temperature response of leaf respiration in Populus deltoides.Crossref | GoogleScholarGoogle Scholar |
Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochimica et Biophysica Acta 1807, 977–988.
| Chlorophyll breakdown in higher plants.Crossref | GoogleScholarGoogle Scholar | 21167811PubMed |
Keech O, Pesquet E, Ahad A, Askne A, Nordvall DAG, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardeström P (2007) The different fates of mitochondria and chloroplasts during dark‐induced senescence in Arabidopsis leaves. Plant, Cell & Environment 30, 1523–1534.
| The different fates of mitochondria and chloroplasts during dark‐induced senescence in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVyjsbfM&md5=f854072c2c2d639027a566d151350b2dCAS |
Kitajima K, Fox AM, Sato T, Nagamatsu D (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biological Invasions 8, 1471–1482.
| Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata.Crossref | GoogleScholarGoogle Scholar |
Law BE, Ryan MG, Anthoni PM (1999) Seasonal and annual respiration of a ponderosa pine ecosystem. Global Change Biology 5, 169–182.
| Seasonal and annual respiration of a ponderosa pine ecosystem.Crossref | GoogleScholarGoogle Scholar |
Myers JA, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. Journal of Ecology 95, 383–395.
| Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVeitb4%3D&md5=bfee2ac9c80c15dc81fc042ed9c72ac3CAS |
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.
| Different regulation of leaf respiration between Spinacia oleracea, a sun species, and Alocasia odora, a shade species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsFejsLo%3D&md5=443f21f513ead290e4667e299f579c91CAS |
Penning de Vries FWT, Brunsting AHM, van Laar HH (1974) Products, requirements and efficiency of biosynthesis: a quantitative approach. Journal of Theoretical Biology 45, 339–377.
| Products, requirements and efficiency of biosynthesis: a quantitative approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXkvVyjt74%3D&md5=eaccaaf8a13ac86cba47650d1220a9ceCAS |
Percival DC, Proctor JTA, Tsujita MJ (1996) Whole-plant net CO2 exchange of raspberry as influenced by air and root-zone temperature, CO2 concentration, irradiation, and humidity. Journal of the American Society for Horticultural Science 121, 838–845.
R Development Core Team (2013) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna)
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.
| Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status.Crossref | GoogleScholarGoogle Scholar | 14871734PubMed |
Sims DA, Gebauer RLE, Pearcy RW (1994) Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance – II. Simulation of carbon balance and growth at different photon flux densities. Plant, Cell & Environment 17, 889–900.
| Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance – II. Simulation of carbon balance and growth at different photon flux densities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFOgtLk%3D&md5=e1c2e1ac487cbe4d63aae8b8de3f5c32CAS |
Slot M, Kitajima K (2015) General patterns of thermal acclimation of leaf respiration across biomes and plant types. Oecologia 177, 885–900.
| General patterns of thermal acclimation of leaf respiration across biomes and plant types.Crossref | GoogleScholarGoogle Scholar | 25481817PubMed |
Slot M, Zaragoza-Castells J, Atkin OK (2008) Transient shade and drought have divergent impacts on the temperature sensitivity of dark respiration in leaves of Geum urbanum. Functional Plant Biology 35, 1135–1146.
| Transient shade and drought have divergent impacts on the temperature sensitivity of dark respiration in leaves of Geum urbanum.Crossref | GoogleScholarGoogle Scholar |
Slot M, Wright SJ, Kitajima K (2013) Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest. Tree Physiology 33, 505–515.
| Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest.Crossref | GoogleScholarGoogle Scholar | 23592296PubMed |
Slot M, Rey‐Sánchez C, Winter K, Kitajima K (2014a) Trait‐based scaling of temperature‐dependent foliar respiration in a species‐rich tropical forest canopy. Functional Ecology 28, 1074–1086.
| Trait‐based scaling of temperature‐dependent foliar respiration in a species‐rich tropical forest canopy.Crossref | GoogleScholarGoogle Scholar |
Slot M, Rey‐Sánchez C, Gerber S, Lichstein JW, Winter K, Kitajima K (2014b) Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance. Global Change Biology 20, 2915–2926.
| Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance.Crossref | GoogleScholarGoogle Scholar | 24604769PubMed |
Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q 10. Global Change Biology 7, 223–230.
| Modelling respiration of vegetation: evidence for a general temperature-dependent Q 10.Crossref | GoogleScholarGoogle Scholar |
Tjoelker MG, Oleksyn J, Reich PB, Żytkowiak 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 |
Turgeon R (1989) The sink–source transition in leaves. Annual Review of Plant Biology 40, 119–138.
| The sink–source transition in leaves.Crossref | GoogleScholarGoogle Scholar |
Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences 14, 6805–6847.
| Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslCnurk%3D&md5=9cd53d8deefbc82dd53d9be888989cc4CAS | 23531539PubMed |
Vanlerberghe GC, McIntosh L (1997) Alternative oxidase: from gene to function. Annual Review of Plant Physiology and Plant Molecular Biology 48, 703–734.
| Alternative oxidase: from gene to function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1eku70%3D&md5=d97cf30494d7379f176c9a8b5cb95d61CAS | 15012279PubMed |
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
| The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFShsbY%3D&md5=dc6c8d091d1effa4ddc2d018f7f9f103CAS |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
