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Modelling the Components of Plant Respiration~Zsome Guiding Annals of Botany 85: 45–54, 2000 Article No. anbo.1999.0996, available online at http:\\www.idealibrary.com on Modelling the Components of Plant Respiration: Some Guiding Principles M.G.R.CANNELL* and J.H.M.THORNLEY Institute of Terrestrial Ecology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK Received: 11 June 1999 Returned for revision: 28 July 1999 Accepted: 20 September 1999 Respiration is poorly represented in whole plant or ecosystem models relative to photosynthesis. This paper reviews the principles underlying the development of a more mechanistic approach to modelling plant respiration and the criteria by which model behaviour might be judged. The main conclusions are as follows: (1) Models should separate C substrate from structure so that direct or indirect C substrate dependence of the components of respiration can be represented. (2) Account should be taken of the fact that some of the energy for leaf respiration is drawn from the light reactions of photosynthesis. (3) It is possible to estimate respiration associated with growth, nitrate reduction, symbiotic N# fixation, N-uptake, other ion uptake and phloem loading, because reasonable estimates are available of average specific unit respiratory costs and the rates of these processes can be quantified. (4) At present, it is less easy to estimate respiration associated with protein turnover, maintenance of cell ion concentrations and gradients and all forms of respiration involving the alternative pathway and futile cycles. (5) The growth-maintenance paradigm is valuable but ‘maintenance’ is an approximate concept and there is no rigorous division between growth and maintenance energy-requiring processes. (6) An alternative ‘process-residual’ approach would be to estimate explicitly respiratory fluxes associated with the six processes listed in (3) above and treat the remainder as a residual with a phenomenological ‘residual maintenance’ coefficient. (7) Maintenance or ‘residual maintenance’ respiration rates are often more closely related to tissue N content than biomass, volume or surface area. (8) Respiratory fluxes associated with different processes vary independently, seasonally and during plant development, and so should be represented separately if possible. (9) An unforced outcome of mechanistic models should be a constrained, but non-constant, ratio between whole plant gross photosynthesis and respiration. # 2000 Annals of Botany Company Key words: Respiration, photosynthesis, growth, maintenance, substrate, N uptake, nitrate reduction, symbiotic N# fixation, phloem loading, model. underlying mechanisms. Respiration is a very large flux; it INTRODUCTION is intimately linked to many other processes—growth, The need to predict the effect of climate change is promoting allocation, nitrogen uptake etc.—and is important in a critical re-examination of ecosystem models, which are determining net primary production and plant death. Broad- ultimately the only tools we have to forecast the effect of brush approaches, which ignore mechanisms, may make it gradual change over decadal timescales. Empirical or more impossible to detect and evaluate a range of possible mechanistic models of photosynthesis enable gross photo- responses and may fail to predict important effects. synthesis to be predicted with some confidence (e.g. Second, there have recently been some theoretical and Farquhar et al., 1980; Cannell and Thornley, 1998). But experimental advances in understanding respiration, e.g. by having estimated assimilate production quite accurately, Ryan and coworkers (Ryan, 1991, 1995; Ryan et al., 1996a, most models then dispense with about half of the assimilate 1997), Bouma and coworkers (Bouma, 1995; Bouma et al., in respiration and allocate the remainder for the growth 1995; 1996) and Gifford (1994, 1995). There is now of plant parts using somewhat arbitrary coefficients or sufficient new information to justify a re-evaluation of the proportions based on widely-ranging observed values (e.g. old concept of growth and maintenance respiration A/ gren et al., 1991; Ryan et al., 1996b). In the most (McCree, 1970; Thornley, 1970) developed by Thornley extreme case, respiration is simply subtracted as a fixed (1977), subsequently extended to include ion uptake by fraction of gross photosynthesis (Coops et al., 1998; Johnson (1983, 1990) and still almost universally adopted as Waring et al., 1998). the paradigm for representing respiration in models This, and the following paper (Thornley and Cannell, (Amthor, 1994, gives an excellent modern statement of this 2000), re-examines the principles and practice of modelling paradigm). plant respiration, with the following two convictions. First, In this paper, we use the recent literature on plant confidence in predicting future ecosystem responses, as respiration to highlight some of the principles that need to opposed to describing past data, may be improved by be considered when developing more mechanistic representing respiration, at least partially, in terms of approaches to plant respiration. We also identify some of the essential observations that models must be capable of simulating. This account draws information from * For correspondence. Fax j44(0)1314453943, e-mail mgrc! recent reviews of respiration, which offer more compre- ite.ac.uk hensive descriptions of the literature (Lambers et al., 0305-7364\00\010045j10 $35.00\0 # 2000 Annals of Botany Company 46 Cannell and Thornley—Modelling the Components of Plant Respiration 1983; Amthor, 1984, 1986, 1991, 1994; Farrar, 1985; uptake and protein resynthesis). Consequently, we should Ryan, 1991; Poorter and Villar, 1997; Reich et al., 1998a, expect the overall demand for ATP and NAD(P)H and b). The companion paper (Thornley and Cannell, 2000) hence the respiration rate to be positively correlated with then re-examines how respiration is represented in models the supply rate and\or concentration of C substrates in and how it may be represented more mechanistically, taking the plant (Farrar, 1985, pp. 432–433; Amthor, 1994, into account the principles outlined below. pp. 508–509). A brief discussion of our assumptions regarding glucose dissimilation, ATP and NADPH production and the P\O RESPIRATION IS CONTROLLED BY BOTH ratio is given in the Appendix. ENERGY DEMAND AND THE SUPPLY OF C SUBSTRATES RESPIRATORY COSTS IN LEAVES MAY BE LESS THAN EXPECTED FROM THEIR MASS Mitochondrial respiration consumes C substrates (mostly OR N CONTENT glucose) to provide energy (ATP) and reducing power (NAD(P)H) for all energy-requiring processes in plants. Figure 1 shows that ATP and NAD(P)H can also be drawn Figure 1 presents a simplified scheme of the way in which directly from the light reaction of photosynthesis. This C substrates are used to generate ATP and NAD(P)H in occurs in chloroplasts during the day when there is excess support of growth and other processes. ATP production and can supply at least part of the energy Assuming that the enzymes involved in respiration are required for growth, protein turnover and phloem loading present in excess, rates of respiration may be viewed as in leaves without consuming C substrates (Raven, 1976; being co-limited by the rate of supply of C substrates (source Lawlor, 1987). In effect, excess energy in the chloroplasts is or ‘push’ limited) and by the demand for ATP and used directly to support respiration, avoiding the need to NAD(P)H by energy-requiring processes, reflected in the synthesize sugars and then respire them. Also, during the rate of supply of ADP and NAD(P) (sink or ‘pull’ limited) night, photosynthetic proteins are not activated, so it is (Farrar, 1985; Amthor, 1994). In growing plants, the rates likely that less ATP is required for protein maintenance. of most processes requiring ATP or NAD(P)H are them- Thus, the consumption of C substrates for respiration in selves dependent on the rate of supply of C substrates either leaves may be less than expected from their mass or N directly (growth and phloem loading) or indirectly (ion content. Allowance should be made for this in models, e.g. Photosynthesis C substrate (glucose) CO C skeletons 2 (glucose) Respiration for growth Direct (Photosynthesis) ADP ATP growth NAD(P), Pi NAD(P)H resp- iration Nitrate reduction (G) N fixation (G) N uptake (G, M) Other ion uptake (G, M) Phloem loading (G, M) Protein (macromolecular) resynthesis (M) Cell ion concs/gradients (M) Alternative pathway, futile cycles (W) Plant tissue Litter (cellulose) F. 1. Simplified scheme of the carbon biochemistry of growth and respiration. Arrows indicate fluxes. G, Growth; M, maintenance; W, wastage respiration. Cannell and Thornley—Modelling the Components of Plant Respiration 47 by adjusting foliage growth and maintenance respiration Thornley and Johnson, 1990, p. 352). For most vegetative n coefficients according to current photosynthetic activity. plant tissue, the growth yield YG is in the range 0 7to 0n85 (this is taking account of the direct construction cost only) equivalent to construction costs or glucose require- PROCESSES WITH QUANTIFIABLE ments in the range 1n2to1n4 g glucose (g dry matter)−" n n RESPIRATORY FLUXES: GROWTH, and CO# production coefficients in the range 0 2to04g −" NITRATE REDUCTION, N# FIXATION, CO# (g dry matter) . N UPTAKE, OTHER ION UPTAKE AND For the construction of organic acids with their low n PHLOEM LOADING energy content (high oxidation state), YG can range from 1 0 to 2n4 g C in organic acid product per g C in glucose At least nine plant processes can be separated which require n energy: growth (Penning de Vries et al., 1983; Thornley substrate, with a value of 1 4 for malate. Equivalent values and Johnson, 1990); nitrate reduction, symbiotic dinitrogen of YG, in units of g C in product per g C in glucose substrate are 0n85 to 1n0 for carbohydrates, 0n8to0n85 for lignins, 0n7 fixation (Simpson, 1987); root N-uptake (Bloom et al., n n 1992); other ion uptake (Thornley and Johnson, 1990, p. for lipids (palmitate), and 0 5to08 for proteins and nucleic 348); phloem loading (Geiger, 1975; Bouma, 1995), protein acids, depending on whether the nitrogen source is ammo- turnover (Vierstra, 1993); maintenance of cell ion con- nium or nitrate.
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