Planta

, Volume 224, Issue 3, pp 680–691

Water stress impacts on respiratory rate, efficiency and substrates, in growing and mature foliage of Eucalyptus spp

Original Article

Abstract

In previous studies, water stress has induced variable and sometimes contradictory changes in respiration. We used isothermal calorimetry to measure the response of foliar respiration to water deficit in nine eucalypt genotypes. Specific growth rates (RSG) of shoots and leaves of variable age were measured independently, and the data were applied to both the growth-maintenance and enthalpy balance models. We calculated the oxidation state of respiratory substrate and the enthalpy change for the conversion of substrate carbon to biomass (ΔHB). Moderate water stress reduced the RSG of shoots by 38% (P<0.01) and carbon conversion efficiency by 15% (P<0.05). The relationship between carbon conversion efficiency and RSG was not affected by water deficit for shoots, but was significantly altered for leaves. Water deficit increased maintenance respiration by about 23% (P<0.001). The growth coefficient of respiration was not significantly altered. However, changes in oxidation states of substrate and biomass suggest that the energy requirements of biosynthesis were increased under water stress. Our results confirm that carbohydrates are the major respiratory substrates in growing tissues, though mature leaves utilized a substantial component of more reduced substrate. Mature leaves had variable oxidation states for respiration substrate, which indicates a variable relationship between CO2 evolution and ATP production. Measured ΔHB in shoots and leaves were too small for reliable estimation of RSG by the enthalpy balance model. We also found significant effects of water stress on the oxidation state of substrate and ΔHB.

Keywords

Calorimetry Eucalyptus Oxidation state Respiration Substrate Water stress 

Abbreviations

ΔHB

Enthalpy change for conversion of substrate carbon to biomass

\( \Delta H_{{{\text{O}}_{2} }} \)

Enthalpy change for catabolism of carbon substrate per mol O2 consumed

εC

Carbon conversion efficiency

g

Growth coefficient of respiration

γB

Oxidation state of biomass

γS

Oxidation state of respiratory substrate

m

Maintenance coefficient of respiration

P/O

Ratio of oxidative phosphorylation to oxygen consumption

RATP

Specific rate of ATP production

\( R_{{{\text{CO}}_{{\text{2}}} }} \)

Specific rate of CO2 evolution

\( R_{{{\text{O}}_{2} }} \)

Sspecific rate of O2 consumption

Rq

Specific rate of heat evolution

RSG

Specific growth rate

References

  1. Amthor JS (1989) Respiration and crop productivity. Springer, Berlin Heidelberg New York, pp 215Google Scholar
  2. Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann Bot 86:1–20CrossRefGoogle Scholar
  3. Amthor JS, McCree KJ (1990) Carbon balance of stressed plants: a conceptual model for integrating research results. In: Alscher RG, Cumming JR (eds) Stress responses in plants: adaptations and acclimation mechanisms. Wiley-Liss, Inc., New York, pp 1–15Google Scholar
  4. Anekonda TS, Adams WT (2000) Genetics of dark respiration and its relationship with drought hardiness in coastal douglas fir. Thermochim Acta 349:69–77CrossRefGoogle Scholar
  5. Anekonda TS, Criddle RS, Bacca M, Hansen LD (1999) Contrasting adaptation of two Eucalyptus subgenera is related to differences in respiratory metabolism. Funct Ecol 13:675–682CrossRefGoogle Scholar
  6. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351CrossRefPubMedGoogle Scholar
  7. Bouma TJ, de Visser R, Janssen JHJA, de Kock MJ, van Leewen PH, Lambers H (1994) Respiratory energy requirements and rate of protein turnover in vivo determined by the use of an inhibitor of protein synthesis and a probe to assess its affect. Physiol Plant 92:585–594CrossRefGoogle Scholar
  8. Bouma TJ, de Visser R, van Leewen 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. J Exp Bot 46:1185–1194CrossRefGoogle Scholar
  9. Boyer JS (1996) Advances in drought tolerance in plants. Adv Agron 56:187–218Google Scholar
  10. Breeze V, Elston J (1983) Examination of a model and data describing the effect of temperature on the respiration rate of crop plants. Ann Bot 51:611–616Google Scholar
  11. Brouquisse R, Gaudillere JP, Raymond P (1998) Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol 117:1281–1291CrossRefPubMedGoogle Scholar
  12. Brown KW, Thomas JC (1980) The influence of water stress preconditioning on dark respiration. Physiol Plant 49:205–209CrossRefGoogle Scholar
  13. Bunce JA (1976) Differential effects of water stress on respiration in the light in woody plants from wet and dry habitats. Can J Bot 54:2457–2464Google Scholar
  14. Cannell MGR, Thornley JHM (2000) Modelling the components of plant respiration: Some guiding principles. Ann Bot 85:45–54CrossRefGoogle Scholar
  15. Causton DR, Venus JC (1981) The biometry of plant growth. Edward Arnold, London, pp 307Google Scholar
  16. Cooke RA, Oliver J, Davies DD (1979) Stress and protein turnover in Lemna minor. Physiol Plant 64:1109–1113CrossRefGoogle Scholar
  17. Criddle RS, Breidenbach RW, Rank DR, Hopkin MS, Hansen LD (1990) Simultaneous calorimetric and respirometric measurements on plant tissues. Thermochim Acta 172:213–221CrossRefGoogle Scholar
  18. Criddle RS, Hansen LD (1999) Calorimetric methods for analysis of plant metabolism. In: Kemp RB (ed) Handbook of thermal analysis and calorimetry, vol 4: from macromolecules to man. Elsevier, Amsterdam, pp 711–763Google Scholar
  19. Criddle RS, Smith BN, Hansen LD (1997) A respiration based description of plant growth rate responses to temperature. Planta 201:441–445CrossRefGoogle Scholar
  20. Dieuaide-Noubhani M, Canioni P, Raymond P (1997) Sugar-starvation-induced changes of carbon metabolism in excised maize root tips. Plant Physiol 115:1505–1513PubMedGoogle Scholar
  21. Dubé PA, Stevenson KR, Thurtell GW, Hunter RB (1975) Effects of water stress on leaf respiration, transpiration rates in the dark and cuticular resistance to water vapor diffusion of two corn inbreds. Can J Plant Sci 55:565–572CrossRefGoogle Scholar
  22. Ellingson D, Olson A, Matheson S, Criddle RS, Smith BN, Hansen LD (2003) Determination of the enthalpy change for anabolism by four methods. Thermochim Acta 400:79–85CrossRefGoogle Scholar
  23. Flexas J, Galmes J, Ribas-Carbo M, Medrano H (2005) The effects of water stress on plant respiration. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem. Springer, Dordrecht, pp 85–94Google Scholar
  24. Ghashghaie J, Badeck F-W, Lanigan G, Nogués S, Tcherkez G, Deléens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochem Rev 2:145–161CrossRefGoogle Scholar
  25. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
  26. Hansen LD, Breidenbach RW, Smith BN, Hansen JR, Criddle RS (1998) Miconceptions about the relation between plant growth and respiration. Bot Acta 111:255–260Google Scholar
  27. Hansen LD, Hopkin MS, Rank DR, Anekonda TS, Breidenbach RW, Criddle RS (1994) The relation between plant growth and respiration: a thermodynamic model. Planta 194:77–85CrossRefGoogle Scholar
  28. Hansen LD, Macfarlane C, McKinnon N, Smith BN, Criddle RS (2004) Use of calorespirometric ratios, heat per CO2 and heat per O2, to quantify metabolic paths and energetics of growing cells. Thermochim Acta 422:55–61CrossRefGoogle Scholar
  29. Hanson AD, Hitz WD (1982) Metabolic responses of mesophytes to plant water deficits. Ann Rev Plant Physiol 33:163–203CrossRefGoogle Scholar
  30. Hitz WD, Ladyman JAR, Hanson AD (1982) Betaine synthesis and accumulation in barley during field water-stress. Crop Sci 22:47–54CrossRefGoogle Scholar
  31. Jeffrey SJ, Carter JO, Moodie KM, Beswick AR (2001) Using spatial interpolation to construct a comprehensive archive of Australian climate data. Environ Model Softw 16:309–330CrossRefGoogle Scholar
  32. John JA, Williams ER (1995) Cyclic and computer generated designs. Chapman & Hall, London, pp 255Google Scholar
  33. Judd TS, Attiwill PM, Adams MA (1996) Nutrient concentrations in Eucalyptus: a synthesis in relation to differences between taxa, sites and components. In: Attiwill PM, Adams MA (eds) Nutrition of eucalypts. CSIRO Publishing, pp 123–154Google Scholar
  34. Lawlor DW (1976) Water stress induced changes in photosynthesis, photorespiration, respiration and CO2 compensation concentration of wheat. Photosynthetica 10:378–387Google Scholar
  35. Lawlor DW, Fock H (1975) Photosynthesis and photorespiratory CO2 evolution of water-stressed sunflower leaves. Planta 126:247–258CrossRefGoogle Scholar
  36. Loomis RS, Lafitte HR (1987) The carbon economy of a maize crop exposed to elevated CO2 concentrations and water stress, as determined from elemental analyses. Field Crops Res 17:63–74CrossRefGoogle Scholar
  37. 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. Proc Roy Soc Lond Ser B 269:1499–1507CrossRefGoogle Scholar
  38. Macfarlane C, Hansen LD, Edwards J, White DA, Adams MA (2005) Growth efficiency increases as relative growth rate increases in shoots and roots of Eucalyptus globulus deprived of nitrogen or treated with salt. Tree Physiol 25:571–582PubMedGoogle Scholar
  39. Marcar NE, Criddle RS, Guo J, Zohar Y (2002) Analysis of respiratory metabolism correlates well with the response of Eucalyptus camaldulensis seedlings to NaCl and high pH. Funct Plant Biol 29:925–932CrossRefGoogle Scholar
  40. Matheson S, Ellingson DJ, McCarlie VW, Smith BN, Criddle RS, Rodier L, Hansen LD (2004) Determination of growth and maintenance coefficients by calorespirometry. Funct Plant Biol 31:929–939CrossRefGoogle Scholar
  41. McArdle BH (1988) The structural relationship: regression in biology. Can J Zool 66:2329–2339CrossRefGoogle Scholar
  42. McCree KJ (1986) Whole-plant carbon balance during osmotic adjustment to drought and salinity stress. Aust J Plant Physiol 13:33–43CrossRefGoogle Scholar
  43. McDermitt DK, Loomis RS (1981) Elemental composition of biomass and its relation to energy content, growth efficiency, and growth yield. Ann Bot 48:275–290Google Scholar
  44. Moldau H, Rahi M (1983) Enhancement of maintenance respiration under water stress. In: Marcelle R, Clijsters H, van Poucke M (eds) Effects of stress on photosynthesis. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, pp 121–132Google Scholar
  45. Moldau KA, Syber YK, Rakhi MO (1980) Components of dark respiration in bean under conditions of a water deficit. Soviet Plant Physiol 27:1–6Google Scholar
  46. Penning de Vries FWT (1975) The cost of maintenance processes in plant cells. Ann Bot 39:77–92Google Scholar
  47. Penning de Vries FWT, Brunsting AHM, van Laar HH (1974) Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol 45:339–377CrossRefPubMedGoogle Scholar
  48. Ribas-Carbo 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 leaves. Plant Physiol 139:466–473CrossRefPubMedGoogle Scholar
  49. Ryan MG (1995) Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content. Plant Cell Environ 18:765–772CrossRefGoogle Scholar
  50. Ryan MG, Hubbard RM, Pongracic S, Raison RJ, McMurtie RE (1996) Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status. Tree Physiol 16:333–343PubMedGoogle Scholar
  51. Taiz L, Zeiger E (1998) Plant physiology. Sinauer Associates, Sunderland, pp 792Google Scholar
  52. Taylor DK, Rank DR, Keiser DR, Smith BN, Criddle RS, Hansen LD (1998) Modelling temperature effects on growth-respiration relations of maize. Plant Cell Environ 21:1143–1151CrossRefGoogle Scholar
  53. Tcherkez G, Nogués S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in french bean. Plant Physiol 131:237–244CrossRefPubMedGoogle Scholar
  54. Thornley JHM, Cannell MGR (2000) Modelling the components of respiration: Representation and realism. Ann Bot 85:55–67CrossRefGoogle Scholar
  55. Thornley JHM, Johnson IR (1990) Plant and crop modeling: a mathematical approach to plant and crop physiology. Oxford University Press, OxfordGoogle Scholar
  56. Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734Google Scholar
  57. Wilson DR, van Bavel CHM, McCree KJ (1980) Carbon balance of water-deficit grain sorghum plants. Crop Sci 20:153–159CrossRefGoogle Scholar
  58. Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol 15:423–434CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.School of Forest and Ecosystem ScienceUniversity of MelbourneCreswickAustralia
  2. 2.Centre of Excellence in Natural Resource ManagementUniversity of Western AustraliaCrawleyAustralia

Personalised recommendations