Determination of growth and maintenance coefficients by calorespirometry
Sannali Matheson A D , Derek J. Ellingson A , V. Wallace McCarlie A , Bruce N. Smith B , Richard S. Criddle A , Laurence Rodier C and Lee D. Hansen AA Department of Chemistry and Biochemistry, Brigham Young University, Provo, UT 84602, USA.
B Department of Plant and Animal Science, Brigham Young University, Provo, UT 84602 USA.
C Laboratoire de Thermodynamique et Genie Chimique, Universite Blaise Pascal, F-63177 Aubiere Cedex, France.
D Corresponding author; email: Lee_Hansen@BYU.edu
Functional Plant Biology 31(9) 929-939 https://doi.org/10.1071/FP03029
Submitted: 7 February 2003 Accepted: 3 June 2004 Published: 27 September 2004
Abstract
This study describes a calorespirometric method for determining the coefficients of the correlation of specific respiration and growth rates. To validate the calorespirometric method, coefficients obtained from calorespirometric data are compared with coefficients obtained from mass and elongation growth rates measured at three temperatures on oat (Avena sativa L.) shoots. Calorespirometric measurements were also made on leaf tissue of varying age from Verbascum thapsus L., Convolvulus arvensis L., and Helianthus tuberosus Nutt. Measurements on A. sativa, C. arvensis and H. tuberosus at several temperatures show maintenance coefficients generally increase with temperature, but, in disagreement with accepted theory, growth coefficients for C. arvensis and A. sativa vary with temperature. A comparison of rates expressed as intensive and extensive quantities showed that the decline in specific respiration and growth rates with age is caused by dilution-by-growth, not down-regulation of respiration rate by reduced demand. The ratio of heat rate to CO2 rate increases with leaf age, and, for fully mature leaves, exceeds the maximum possible value for carbohydrates. This shows that the catabolic substrate may vary with leaf age in immature leaves and cannot be assumed to consist only of carbohydrates in mature leaves. Dilution-by-growth, substrate variation, and inseparability of the variables in the growth-maintenance model all complicate physiological interpretation of the slope and intercept of plots of specific respiration rates v. specific growth rates.
Keywords: Avena sativa, calorimetry, Convolvulus arvensis, Helianthus tuberosa, models, respiration, Verbascum thapsus.
Acknowledgments
S Matheson thanks the BYU Office of Research and Creative Activities for a grant in support of this research. L D Hansen thanks CNRS for support through the Laboratoire de Thermodynamique et Génie Chimique of the Université Blaise Pascal, Clermont-Ferrand, France for time to perform the initial studies on verbascum that led to this work, the Forestry Research Laboratory of the University of Melbourne and the Botany Department of the University of Western Australia for time to write the manuscript, and BYU for continued support of this work.
Amthor, JS (1989).
Amthor JS
(2000) The McCree–de Wit–Penning de Vries–Thornley respiration paradigms: 30 years later. Annals of Botany 86, 1–20.
| Crossref | GoogleScholarGoogle Scholar |
Battley EH
(1999) The thermodynamics of microbial growth. ‘Handbook of thermal analysis and calorimetry. Vol. 4’. (Ed. RB Kemp)
pp. 219–266. (Elsevier: Amsterdam, The Netherlands)
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 |
Cannell MGR, Thornley JHM
(2000) Modelling the components of plant respiration: some guiding principles. Annals of Botany 85, 45–54.
| Crossref | GoogleScholarGoogle Scholar |
Chiariello NR, Mooney HA, Williams K
(1989) Growth, carbon allocation and cost of plant tissues. ‘Plant physiological ecology’. (Eds RW Pearcy, JR Ehleringer, HA Mooney, PW Rundel)
pp. 327–365. (Chapman and Hall: London, UK)
Criddle RS,
Church JN,
Smith BN, Hansen LD
(2003) Fundamental causes of the global patterns of species range and richness. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 192–199.
| Crossref | GoogleScholarGoogle Scholar |
Criddle RS, Hansen LD
(1999) Calorimetric methods for analysis of plant metabolism. ‘Handbook of thermal analysis and calorimetry. Vol. 4’. (Ed. RB Kemp)
pp. 711–732. (Elsevier: Amsterdam, The Netherlands)
Criddle RS,
Smith BN, Hansen LD
(1997) A respiration based description of plant growth rate responses to temperature. Planta 201, 441–445.
| Crossref | GoogleScholarGoogle Scholar |
Earl HJ, Tollenaar M
(1998) Differences among commercial maize (Zea mays L.) hybrids in respiration rates of mature leaves. Field Crops Research 59, 9–19.
| Crossref | GoogleScholarGoogle Scholar |
Ellingson D,
Olson A,
Matheson S,
Criddle RS,
Smith BN, Hansen LD
(2003) Determination of the enthalpy change for anabolism by four methods. Thermochimica Acta 400, 79–85.
| Crossref | GoogleScholarGoogle Scholar |
Evans, LT (1993).
Fitter, AH ,
and
Hay, RKM (1987).
Gary C,
Frossard JS, Chenevard D
(1995) Heat of combustion, degree of reduction and carbon content: 3 interrelated methods of estimating the construction cost of plant tissues. Agronomie 15, 59–69.
Gary C,
le Bot J,
Frossard J-S, Andriolo JL
(1998) Ontogenic changes in the construction cost of leaves, stems fruits, and roots of tomato plants. Journal of Experimental Botany 49, 59–68.
| Crossref | GoogleScholarGoogle Scholar |
Gifford RM
(2002) Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research. Functional Plant Biology 30, 171–186.
| Crossref | GoogleScholarGoogle Scholar |
Hansen LD,
Breidenbach RW,
Smith BN,
Hansen JR, Criddle RS
(1998) Misconceptions about the relation between plant growth and respiration. Botanica Acta 4, 255–260.
Hansen LD,
Macfarlane C,
McKinnon N,
Smith BN, Criddle RS
(2004a) Use of calorespirometric ratios, heat per CO2 and heat per O2, to quantify metabolic paths and energetics of growing cells. Thermochimica Acta, in press ,
Hansen LD, Criddle RS, Smith BN
(2004b) Calorespirometry in plant biology. ‘Plant respiration’. In press,(Eds M Ribas-Carbo, H Lambers)
(Kluwer: Dordrecht, The Netherlands)
Hesketh JD,
Ogren WL,
Hageman ME, Peters DB
(1981) Correlations among leaf CO2-exchange rates, areas and enzyme activities among soybean cultivars. Photosynthesis Research 2, 21–30.
Körner C
(1989) The nutritional status of plants from high altitudes. A worldwide comparison. Oecologia 81, 379–391.
Körner C
(1998) A reassessment of high elevation treeline positions and their explanation. Oecologia 115, 445–459.
| Crossref | GoogleScholarGoogle Scholar |
Lambers, H ,
Chapin, FS ,
and
Pons, TL (1998).
Lambers H, Chapin FS, Pons TL
(2002) Respiration and lipid metabolism. ‘Plant physiology online’. (Available on line at http: //www.plantphys.net/article.php?ch=11&id=152)
Lawlor DW
(1995) Photosynthesis, productivity and environment. Journal of Experimental Botany 46, 1449–1461.
Loomis RS, Amthor JS
(1999) Yield potential, plant assimilatory capacity, and metabolic efficiencies. Crop Science 39, 1584–1596.
Macfarlane C,
Adams MA, Hansen LD
(2002) Application of an enthalpy balance model of the relation between growth and respiration to temperature acclimation of Eucalyptus globulus seedlings. Proceedings of the Royal Society of London. Series B. Biological Sciences 269, 1499–1507.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marcar NE,
Criddle RS,
Guo J, Zohar Y
(2002) Analysis of respiratory metabolism with the response of Eucalyptus camaldulensis seedlings to NaCl and high pH. Functional Plant Biology 29, 925–932.
| Crossref | GoogleScholarGoogle Scholar |
McCree KJ
(1970) An equation for the rate of respiration of white clover plants grown under controlled conditions. ‘Prediction and measurement of photosynthetic productivity’. (Ed. I Setlik)
pp. 221–229. (PUDOC: Wageningen, Germany)
Penning de Vries FWT
(1975) The cost of maintenance processes in plant cells. Annals of Botany 39, 77–92.
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.
Radford PJ
(1967) Growth analysis formulae — their use and abuse. Crop Science 7, 171–175.
Ryan MG
(1991) Effects of climate change on plant respiration. Ecological Applications 1, 157–167.
Taylor DK,
Rank DR,
Keiser DR,
Smith BN,
Criddle RS, Hansen LD
(1998) Modelling temperature effects on growth–respiration relations of maize. Plant, Cell and Environment 21, 1143–1151.
| Crossref | GoogleScholarGoogle Scholar |
Thornley JHM
(1970) Respiration, growth and maintenance in plants. Nature 227, 304–305.
Thornley JHM, Cannell MGR
(2000) Modelling the components of plant respiration: representation and realism. Annals of Botany 85, 55–67.
| Crossref | GoogleScholarGoogle Scholar |
Thornton WM
(1917) The relation of oxygen to the heat of combustion of organic compounds. Philosophical Magazine 33, 196–203.
Tjoelker MG,
Oleksyn J, Reich PB
(1999) 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 | GoogleScholarGoogle Scholar |
Wilson D
(1975) Variation in leaf respiration in relation to growth and photosynthesis of Lolium. The Annals of Applied Biology 80, 323–338.