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Stores as Substrate Sources of Respiration: Effects of Nitrogen Stress and Day Length

  • C. A. Lehmeier
  • F. A. Lattanzi
  • H. SchnyderEmail author
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 220)

Abstract

Dark respiration is a major drain for carbon substrates in plants. Until recently, little was known about the quantitative importance and functional characteristics of stores as substrate suppliers for plant respiration under stresses. Here we review recent work with Lolium perenne L., a perennial grass, subject to nitrogen stress or regular (diurnal) interruptions of photosynthetic activity. This work responds to the following questions: What is the actual contribution of stores (relative to current photosynthate) to the substrate supply of whole plant respiration? What is the size and what are the kinetic properties of the stores which supply substrate for respiration? How do these characteristics respond to nitrogen stress and day/night cycles? The investigations were performed with continuous 13C labelling of plants, monitoring the kinetics of 13C-tracer appearance in respiratory CO2 and compartmental modelling of the tracer data.

Keywords

Fractional Contribution Respiratory Substrate Nitrogen Stress Specific Respiration Rate Fructan Content 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Amthor JS (1989) Respiration and crop productivity. Springer, New YorkCrossRefGoogle 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. ap Rees T (1980) Assessment of the contribution of metabolic pathways to plant respiration. In: Davies DD (ed) The biochemistry of plants: a comprehensive treatise, vol 2. Academic, San Diego, pp 1–29Google Scholar
  4. Atkins GL (1969) Multicompartment models in biological systems. Methuen, LondonGoogle Scholar
  5. Avice JC, Ourry A, Lemaire G, Boucoud J (1996) Nitrogen and carbon flows estimated by 15N and 13C pulse-chase labeling during regrowth of alfalfa. Plant Physiol 112:281–290PubMedPubMedCentralGoogle Scholar
  6. Borland AM, Farrar JF (1985) Diel patterns of carbohydrate metabolism in leaf blades and leaf sheaths of Poa annua L. and Poa jemtlandica (Almq.) Richt. New Phytol 100:519–531CrossRefGoogle Scholar
  7. Borland AM, Farrar JF (1988) Compartmentation and fluxes of carbon in leaf blades and leaf sheaths of Poa annua L. and Poa x jemtlandica (Almq.) Richt. Plant Cell Environ 11:535–543CrossRefGoogle Scholar
  8. 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 117:1281–1291PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bürkle L, Hibberd JM, Quick WP, Kühn C, Hirner B, Frommer WB (1998) The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol 118:59–68PubMedCrossRefPubMedCentralGoogle Scholar
  10. Davidson JL, Milthorpe FL (1966a) Leaf growth in Dactylis glomerata following defoliation. Ann Bot 30:173–184Google Scholar
  11. Davidson JL, Milthorpe FL (1966b) The effect of defoliation on the carbon balance in Dactylis glomerata. Ann Bot 30:185–198Google Scholar
  12. Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715PubMedCrossRefPubMedCentralGoogle Scholar
  13. Dungey NO, Davies DD (1982) Protein turnover in the attached leaves of non-stressed and stressed barley seedlings. Planta 154:435–440PubMedCrossRefGoogle Scholar
  14. Farrar JF (1989) Fluxes and turnover of sucrose and fructans in healthy and diseased plants. J Plant Physiol 134:137–140CrossRefGoogle Scholar
  15. Farrar SC, Farrar JF (1985) Carbon fluxes in leaf blades of barley. New Phytol 100:271–283CrossRefGoogle Scholar
  16. Farrar SC, Farrar JF (1986) Compartmentation and fluxes of sucrose in intact leaf blades of barley. New Phytol 103:645–657CrossRefGoogle Scholar
  17. Gamnitzer U, Schäufele R, Schnyder H (2009) Observing 13C labelling kinetics in CO2 respired by a temperate grassland ecosystem. New Phytol 184:376–386PubMedCrossRefGoogle Scholar
  18. Gebbing T, Schnyder H, Kühbauch W (1999) The utilization of pre-anthesis reserves in grain filling of wheat. Assessment by steady-state 13CO2/12CO2 labelling. Plant Cell Environ 22:851–858CrossRefGoogle Scholar
  19. Geiger DR, Saunders MA, Cataldo DA (1969) Translocation and accumulation of translocate in the sugar beet petiole. Plant Physiol 44:1657–1665PubMedCrossRefPubMedCentralGoogle Scholar
  20. Gerhardt R, Stitt M, Heldt HW (1987) Subcellular metabolite levels in Spinach leaves – regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol 83:399–407PubMedCrossRefPubMedCentralGoogle Scholar
  21. Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, diurnal starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32:859–874PubMedCrossRefGoogle Scholar
  22. Gifford RM (2003) Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research. Funct Plant Biol 30:171–186CrossRefGoogle Scholar
  23. Graber LF (1931) Food reserves in relation to other factors limiting the growth of grasses. Plant Physiol 6:43–71PubMedCrossRefPubMedCentralGoogle Scholar
  24. Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends Plant Sci 16:169–175PubMedCrossRefGoogle Scholar
  25. Hoch G (2007) Cell wall hemicelluloses as mobile carbon stores in non-reproductive plant tissues. Funct Ecol 21:823–834CrossRefGoogle Scholar
  26. Irving LJ, Robinson D (2006) A dynamic model of Rubisco turnover in cereal leaves. New Phytol 169:493–504PubMedCrossRefGoogle Scholar
  27. Jacquez JA (1996) Compartmental analysis in biology and medicine, 3rd edn. Biomedware, Ann ArborGoogle Scholar
  28. Klumpp K, Schäufele R, Lötscher M, Lattanzi FA, Feneis W, Schnyder H (2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant Cell Environ 28:241–250CrossRefGoogle Scholar
  29. Kouchi H, Nakaji K, Yoneyama T, Ishizuka J (1985) Dynamics of carbon photosynthetically assimilated in nodulated soya bean plants under steady-state conditions. 3. Time-course study on 13C incorporation into soluble metabolites and respiratory evolution of 13CO2 from roots and nodules. Ann Bot 56:333–346Google Scholar
  30. Kouchi H, Akao S, Yoneyama T (1986) Respiratory utilization of 13C-labelled photosynthate in nodulated root systems of soybean plants. J Exp Bot 37:985–993CrossRefGoogle Scholar
  31. Kozlowski TT (1992) Carbohydrate sources and sinks in woody plants. Bot Rev 58:107–222CrossRefGoogle Scholar
  32. Lattanzi FA, Schnyder H, Thornton B (2005) The sources of carbon and nitrogen supplying leaf growth: assessment of the role of stores with compartmental models. Plant Physiol 137:383–395PubMedCrossRefPubMedCentralGoogle Scholar
  33. Lea PJ, Ireland RJ (1999) Nitrogen metabolism in higher plants. In: Singh BK (ed) Plant amino acids. Marcel Dekker, New York, pp 1–47Google Scholar
  34. Lehmeier CA, Lattanzi FA, Schäufele R, Wild M, Schnyder H (2008) Root and shoot respiration of perennial ryegrass are supplied by the same substrate pools: assessment by dynamic 13C labeling and compartmental analysis of tracer kinetics. Plant Physiol 148:1148–1158PubMedCrossRefPubMedCentralGoogle Scholar
  35. Lehmeier CA, Lattanzi FA, Schäufele R, Schnyder H (2010a) Nitrogen deficiency increases the residence time of respiratory carbon in the respiratory substrate supply system of perennial ryegrass. Plant Cell Environ 33:76–87PubMedGoogle Scholar
  36. Lehmeier CA, Lattanzi FA, Gamnitzer U, Schäufele R, Schnyder H (2010b) Day-length effects on carbon stores for respiration of perennial ryegrass. New Phytol 188:719–725PubMedCrossRefGoogle Scholar
  37. Lötscher M, Gayler S (2005) Contribution of current photosynthates to root respiration of non-nodulated Medicago sativa: effects of light and nitrogen supply. Plant Biol 7:601–610PubMedCrossRefGoogle Scholar
  38. Lötscher M, Klumpp K, Schnyder H (2004) Growth and maintenance respiration for individual plants in hierarchically structured canopies of Medicago sativa and Helianthus annuus: the contribution of current and old assimilates. New Phytol 164:305–316CrossRefGoogle Scholar
  39. Makino A, Osmond B (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 96:355–362PubMedCrossRefPubMedCentralGoogle Scholar
  40. Moorby J, Jarman PD (1975) The use of compartmental analysis in the study of the movement of carbon through leaves. Planta 122:155–168PubMedCrossRefGoogle Scholar
  41. Mortazavi B, Conte MH, Chanton JP, Smith MC, Crumsey J, Ghashghaie J (2009) Does the 13C foliage-respired CO2 and biochemical pools reflect the 13C of recently assimilated carbon? Plant Cell Environ 32:1310–1323PubMedCrossRefGoogle Scholar
  42. Morvan-Bertrand A, Boucaud J, Prud’homme MP (1999) Influence of initial levels of carbohydrates, fructans, nitrogen, and soluble proteins on regrowth of Lolium perenne L. cv Bravo following defoliation. J Exp Bot 50:1817–1826CrossRefGoogle Scholar
  43. Motulsky H, Christopoulos A (2004) Fitting models to biological data using linear and nonlinear regression. Oxford University Press, New YorkGoogle Scholar
  44. Muntz K (1998) Deposition of storage proteins. Plant Mol Biol 38:77–99PubMedCrossRefGoogle Scholar
  45. Nogués S, Tcherkez G, Cornic G, Ghashghaie J (2004) Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling. Plant Physiol 136:3245–3254PubMedCrossRefPubMedCentralGoogle Scholar
  46. Penning de Vries FWT (1975) The cost of maintenance processes in plant cells. Ann Bot 39:77–92Google Scholar
  47. Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198CrossRefGoogle Scholar
  48. Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annu Rev Plant Physiol Plant Mol Biol 42:77–101CrossRefGoogle Scholar
  49. Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607CrossRefGoogle Scholar
  50. Prosser J, Farrar JF (1981) A compartmental model of carbon allocation in the vegetative barley plant. Plant Cell Environ 4:303–307Google Scholar
  51. R Development Core Team (2007) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL: http://www.R-project.org
  52. Rescigno A (2001) The rise and fall of compartmental analysis. Pharmacol Res 44:337–342PubMedCrossRefGoogle Scholar
  53. Rocher JP, Prioul JL (1987) Compartmental analysis of assimilate export in a mature maize leaf. Plant Physiol Biochem 25:531–540Google Scholar
  54. Rufty TW, Huber SC, Volk RJ (1988) Alterations in leaf carbohydrate-metabolism in response to nitrogen stress. Plant Physiol 88:725–730PubMedCrossRefPubMedCentralGoogle Scholar
  55. Ryle GJA, Cobby JM, Powell CE (1976) Synthetic and maintenance respiratory losses of 14CO2 in uniculm barley and maize. Ann Bot 40:571–586Google Scholar
  56. Schnyder H (1992) Long-term steady-state labelling of wheat plants by use of natural 13CO2/12CO2 mixtures in an open, rapidly turned-over system. Planta 187:128–135PubMedCrossRefGoogle Scholar
  57. Schnyder H (1993) The role of carbohydrate storage and redistribution in the source-sink relationships of wheat and barley during grain filling – a review. New Phytol 123:233–245CrossRefGoogle Scholar
  58. Schnyder H, Schäufele R, Lötscher M, Gebbing T (2003) Disentangling CO2 fluxes: direct measurements of mesocosm-scale natural abundance 13CO2/12CO2 gas exchange, 13C discrimination, and labelling of CO2 exchange flux components in controlled environments. Plant Cell Environ 26:1863–1874CrossRefGoogle Scholar
  59. Sicher RC, Kremer DF, Harris WG (1984) Diurnal carbohydrate metabolism of barley primary leaves. Plant Physiol 76:165–169PubMedCrossRefPubMedCentralGoogle Scholar
  60. Simpson E, Cooke RJ, Davies DD (1981) Measurement of protein degradation in leaves of Zea mays using [3H]acetic anhydride and tritiated water. Plant Physiol 67:1214–1219PubMedCrossRefPubMedCentralGoogle Scholar
  61. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149PubMedCrossRefGoogle Scholar
  62. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  63. Sullivan JT, Sprague VG (1943) Composition of the roots and stubble of perennial ryegrass following partial defoliation. Plant Physiol 18:656–670PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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 131:237–244PubMedCrossRefPubMedCentralGoogle Scholar
  65. Teixeira EI, Moot DJ, Mickelbart MV (2007) Seasonal patterns of root C and N reserves of lucerne crops (Medicago sativa L.) grown in a temperate climate were affected by defoliation regime. Eur J Agron 26:10–20CrossRefGoogle Scholar
  66. Van Iersel MW (2003) Carbon use efficiency depends on growth respiration, maintenance respiration and relative growth rate: a case study with lettuce. Plant Cell Environ 29:1441–1449CrossRefGoogle Scholar
  67. Volenec JJ, Ourry A, Joern BC (1996) A role for nitrogen reserves in forage regrowth and stress tolerance. Physiol Plant 97:185–193CrossRefGoogle Scholar
  68. Wagner W, Keller F, Wiemken A (1983) Fructan metabolism in cereals: induction in leaves and compartmentation in protoplasts and vacuoles. Zeitschrift für Pflanzenphysiologie 112:359–372CrossRefGoogle Scholar
  69. Windt CW, Vergeldt FJ, de Jager PA, Van As H (2006) MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ 29:1715–1729PubMedCrossRefGoogle Scholar
  70. Winzeler M, Dubois D, Nösberger J (1990) Absence of fructan degradation during fructan accumulation in wheat stems. J Plant Physiol 136:324–329CrossRefGoogle Scholar
  71. Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Lehrstuhl für GrünlandlehreTechnische Universität MünchenFreisingGermany

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