The role of maintenance respiration in plant growth

Abstract Plant growth is the balance of photosynthetic gains and respiratory losses, and it is therefore essential to consider respiration in analyses of plant productivity. The partitioning of dark respiratory losses into two functional components, a growth component and a maintenance component, has proved useful. The growth loss is that associated with synthesis of new biomass while the maintenance loss is that associated with maintenance of existing biomass. Experimental evidence indicates that the respiratory cost of maintenance in herbaceous plants is about equal to the cost of growth over a growing season, with daily maintenace expenditures less important in the small, rapidly growing plant but increasing in significance as plant size increases and the relative growth rate decreases. Because it is such a large fraction of the total carbon budget of a plant, any variations in maintenance requirements may result in significant alterations in productivity. In the present work the theoretical and empirical bases of maintenance respiration are described: magnitudes of maintenance expenditures are summarized; and applications to models of plant growth and productivity are discussed. It is concluded that the costs of maintenance should be included in analyses of plant growth.     

Growth and Maintenance Respiration in Whole Plants, Tops, and Roots of Lolium multiflorum

Continuous measurements of CO₂-exchange were separately carried out on tops and roots of small swards of Lolium multiflorum grown in nutrient solution in growth chamber during 3–4 weeks. From these measurements, a daily carbon balance and accumulated dry matter could be established. The data were used to distinguish between two components of respiration, one proportional to growth or photosynthesis (growth respiration), the other proportional to plant dry weight (maintenance respiration). The separation of respiration in the two components was made by multiple regression analyses with daily photosynthesis or growth rate and accumulated dry matter as the independent variables. To ensure independency between the independent variables during the growth period, photosynthesis was varied by application of alternate three-day periods of high and low irradiance. From the two regression coefficients, the efficiency of converting assimilates into constructive growth (Y_G) and the maintenance coefficient (M) could be derived. Three experiments with varying length of photoperiod and dark period were carried out. The analyses were carried out for whole-plant respiration, respiration of tops and respiration of roots separately. Growth respiration for whole plants as well as for tops and for roots was lower — and hence the efficiencies higher — the longer the photoperiods were. Growth respiration and maintenance respiration were higher for roots than for tops. The high rate of root respiration may originate from release of HCO₃^? in exchange for NO₃^?. The parameters found can be utilized quantitatively in computer models of crop photosynthesis and respiration.     

Modelling the Components of Plant Respiration: Representation and Realism

This paper outlines the different ways in which plant respirationis modelled, with reference to the principles set out in Cannelland Thornley (Annals of Botany85: 55–67, 2000), firstin whole-plant ‘toy’ models, then within ecosystemor crop models using the growth-maintenance paradigm, and finallyrepresenting many component processes within the Hurley Pasture(HPM) and Edinburgh Forest Models (EFM), both of which separateC and N substrates from structure. Whole-plant models can beformulated so that either maintenance or growth respirationtake priority for assimilates, or so that growth respirationis the difference between total respiration and maintenanceassociated with the resynthesis of degraded tissues. All threeschemes can be converted to dynamic models which give similar,reasonable predictions of plant growth and respiration, butall have limiting assumptions and scope. Ecosystem and cropmodels which use the growth-maintenance respiration paradigmwithout separating substrates from structure, implicitly assumethat maintenance respiration is a fixed cost, uncoupled to assimilatesupply, and use fixed rate coefficients chosen from a rangeof measured values. Separation of substrates in the HPM andEFM enables estimates to be made of respiration associated withlocal growth, phloem loading, ammonium and nitrate N uptake,nitrate reduction, N₂fixation and other mineral ion uptake,leaving a ‘residual maintenance’ term. The lattercan be explicitly related to C substrate supply. Simulated changesin grassland respiration over a season and forest respirationover a rotation show that the ratio of total respiration togross canopy photosynthesis varies within the expected limitedrange, that residual maintenance accounts for 46–48% oftotal respiration, growth 36–42%, phloem loading 10–12%and the other components for the small remainder, with the ratiosbetween components varying during a season or forest rotation.It is concluded that the growth-maintenance approach to respiration,extended to represent many of the component processes, has considerablemerit. It can be connected to reality at many points, it givesmore information, it can be examined at the level of assumptionsas well as at the level of predictions, and it is open to modificationas more knowledge emerges. However, currently, there are stillparameters that require adjustment so that the predictions ofthe model are acceptable. Copyright 2000 Annals of Botany Company Respiration, photosynthesis, growth, maintenance, substrate, N uptake, mineral uptake, phloem loading, model.     

Carbon respired by terrestrial ecosystems – recent progress and challenges

Net ecosystem production is the residual of two much larger fluxes: photosynthesis and respiration. While photosynthesis is a single process with a well‐established theoretical underpinning, respiration integrates the variety of plant and microbial processes by which CO₂ returns from ecosystems to the atmosphere. Limits to current capacity for predicting ecosystem respiration fluxes across biomes or years result from the mismatch between what is usually measured – bulk CO₂ fluxes – and what process‐based models can predict – fluxes of CO₂ from plant (autotrophic) or microbial (heterotrophic) respiration. Papers in this Thematic Issue and in the recent literature, document advances in methods for separating respiration into autotrophic and heterotrophic components using three approaches: (1) continuous measurements of CO₂ fluxes and assimilation of these data into process‐based models; (2) application of isotope measurements, particularly radiocarbon; and (3) manipulation experiments. They highlight the role of allocation of C fixed by plants to respiration, storage, growth or transfer to other organisms as a control of seasonal and interannual variability in soil respiration and the oxidation state of C in the terrestrial biosphere. A second theme is the potential for comparing C isotope signatures in organic matter, CO₂ evolved in incubations and microbial biomarkers to elucidate the pathways (respiration, recycling, or transformation) of C during decomposition. Together, these factors determine the continuum of timescales over which C is returned to the atmosphere by respiration and enable testing of theories of plant and microbial respiration that go beyond empirical models and allow predictions of future respiration responses to future change in climate, pollution and land use.     

Kinetics and stoichiometry of growth of plant cell cultures of Catharanthus roseus and Nicotiana tabacum in batch and continuous fermentors

Plant cell suspension cultures of Catharanthus roseus and Nicotiana tabacum were grown in stirred tank bioreactors operated in batch and continuous mode. The stoichiometry of growth of both species in steady-state glucose limited chemostats was studied at a range of different dilution rates. A linear relation was applied to describe specific glucose uptake, oxygen consumption, and carbon dioxide production as a function of the growth rate. Specific respiration deviated greatly from the linear relation. An unstructured mathematical model, based on the observed stoichiometry in the glucose limited chemostats, was applied to describe the growth in batch culture. From a comparison between the observed growth pattern in batch fermentors and computer simulations it appeared that the stoichiometry of growth of the C. roseus culture was different under steady-state and dynamic conditions. It was concluded that a mathematical model for the growth of suspension culture plant cells in which the biomass is considered to be a single compound with an average chemical composition is of limited value because large changes in the conmposition of the biomass may occur. (c) 1992 John Wiley & Sons, Inc.     

Growth, Maintenance and Respiration: a Re-interpretation

The traditional view of respiration being due to the processesof growth and maintenance is questioned. A model is proposedin which plant dry matter is divided into three categories:storage material which may be used for growth; non-degradablestructural material which cannot be recycled, and which is consideredto be inert; and degradable structural material which is assigneda rate constant of degradation, and which is considered to bebiologically active. The model has four parameters: two yieldconstants, and two rate constants, and it has been solved forsteady-state exponential growth in continuous daylight, respirationin the dark, and ^l4CO₂ evolution after a pulse label. Analysisof ^l4CO₂ efflux data leads to the complete definition of themodel. The utility and comparative merits of the suggested viewpointof respiration are discussed.     

Respiration hastens maturation and lowers yield in rice

Role of respiration in plant growth remains an enigma. Growth of meristematic cells, which are not photosynthetic, is entirely driven by endogenous respiration. Does respiration determine growth and size or does it merely burn off the carbon depleting the biomass? We show here that respiration of the germinating rice seed, which is contributed largely by the meristematic cells of the embryo, quantitatively correlates with the dynamics of much of plant growth, starting with the time for germination to the time for flowering and yield. Seed respiration appears to define the quantitative phenotype that contributes to yield via growth dynamics that could be discerned even in commercial varieties, which are biased towards higher yield, despite considerable susceptibility of the dynamics to environmental perturbations. Intrinsic variation, irreducible despite stringent growth conditions, required independent validation of relevant physiological variables both by critical sampling design and by constructing dendrograms for the interrelationships between variables that yield high consensus. More importantly, seed respiration, by mediating the generation clock time via variable time for maturation as seen in rice, directly offers the plausible basis for the phenotypic variation, a major ecological stratagem in a variable environment with uncertain water availability. Faster respiring rice plants appear to complete growth dynamics sooner, mature faster, resulting in a smaller plant with lower yield. Counter to the common allometric views, respiration appears to determine size in the rice plant, and offers a valid physiological means, within the limits of intrinsic variation, to help parental selection in breeding.Key words: Meristematic cells, allometry, flowering, branching     

Plant respiration and elevated atmospheric CO2 concentration: cellular responses and global significance

BACKGROUND: Elevated levels of atmospheric [CO2] are likely to enhance photosynthesis and plant growth, which, in turn, should result in increased specific and whole-plant respiration rates. However, a large body of literature has shown that specific respiration rates of plant tissues are often reduced when plants are exposed to, or grown at, high [CO2] due to direct effects on enzymes and indirect effects derived from changes in the plant's chemical composition. SCOPE: Although measurement artefacts may have affected some of the previously reported effects of CO2 on respiration rates, the direction and magnitude for the effects of elevated [CO2] on plant respiration may largely depend on the vertical scale (from enzymes to ecosystems) at which measurements are taken. In this review, the effects of elevated [CO2] from cells to ecosystems are presented within the context of the enzymatic and physiological controls of plant respiration, the role(s) of non-phosphorylating pathways, and possible effects associated with plant size. CONCLUSIONS: Contrary to what was previously thought, specific respiration rates are generally not reduced when plants are grown at elevated [CO2]. However, whole ecosystem studies show that canopy respiration does not increase proportionally to increases in biomass in response to elevated [CO2], although a larger proportion of respiration takes place in the root system. Fundamental information is still lacking on how respiration and the processes supported by it are physiologically controlled, thereby preventing sound interpretations of what seem to be species-specific responses of respiration to elevated [CO2]. Therefore the role of plant respiration in augmenting the sink capacity of terrestrial ecosystems is still uncertain.     

Responses of respiration to increasing atmospheric carbon dioxide concentrations

It has been recently recognized that increases in carbon dioxide concentration such as are anticipated for the earth's atmosphere in the next century often reduce plant respiration. There can be both a short-term reversible effect of unknown cause, and long-term acclimation, which may reflect the synthesis and maintenance of less metabolically expensive materials in plants grown at elevated carbon dioxide concentrations. Because respiration provides energy and carbon intermediates for growth and maintenance, reductions in respiration by increasing carbon dioxide concentrations may have effects on physiology beyond an improvement in plant carbon balance. As atmospheric carbon dioxide concentration increases, reduced respiration could be as important as increased photosynthesis in improving the ability of terrestrial vegetation to act as a sink for carbon, but it could also have other consequences.     

Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth

Phenolics can reduce soil nutrient availability, either indirectly by stimulating microbial nitrogen (N) immobilization or directly by enhancing physical protection within soil. Phenolic-rich plants may therefore negatively affect neighboring plant growth by restricting the N supply. We used a slow-growing, phenolic-rich alpine forb, Acomastylis rossii, to test the hypothesis that phenolic-rich carbon (C) fractions stimulate microbial population growth and reduce plant growth. We generated low-molecular-weight (LMW) fractions, tannin fractions, and total soluble C fractions from A. rossii and measured their effects on soil respiration and growth of Deschampsia caespitosa, a fast-growing, co-dominant grass. Fraction effects fell into two distinct categories: (1) fractions did not increase soil respiration and killed D. caespitosa plants, or (2) fractions stimulated soil respiration and reduced plant growth and plant N concentration while simultaneously inhibiting root growth. The LMW phenolic-rich fractions increased soil respiration and reduced plant growth more than tannins. These results suggest that phenolic compounds can inhibit root growth directly as well as indirectly affect growth by reducing pools of plant available N by stimulating soil microbes. Both mechanisms illustrate how below-ground phenolic effects may influence the growth of neighboring plants. We also examined patterns of foliar phenolic concentrations among populations of A. rossii across a natural productivity gradient (productivity was used as a proxy for competition intensity). Concentrations of some LMW phenolics increased significantly in more productive sites where A. rossii is a competitive equal with the faster growing D. caespitosa. Taken together, our results contribute important information to the growing body of evidence indicating that the quality of C moving from plants to soils can have significant effects on neighboring plant performance, potentially associated with phytoxic effects, and indirect effects on soil biogeochemistry.     

Plant species richness regulates soil respiration through changes in productivity

Soil respiration is an important pathway of the C cycle. However, it is still poorly understood how changes in plant community diversity can affect this ecosystem process. Here we used a long-term experiment consisting of a gradient of grassland plant species richness to test for effects of diversity on soil respiration. We hypothesized that plant diversity could affect soil respiration in two ways. On the one hand, more diverse plant communities have been shown to promote plant productivity, which could increase soil respiration. On the other hand, the nutrient concentration in the biomass produced has been shown to decrease with diversity, which could counteract the production-induced increase in soil respiration. Our results clearly show that soil respiration increased with species richness. Detailed analysis revealed that this effect was not due to differences in species composition. In general, soil respiration in mixtures was higher than would be expected from the monocultures. Path analysis revealed that species richness predominantly regulates soil respiration through changes in productivity. No evidence supporting the hypothesized negative effect of lower N concentration on soil respiration was found. We conclude that shifts in productivity are the main mechanism by which changes in plant diversity may affect soil respiration.     

Analysis of double-substrate limited growth

Mathematical models which relate the growth rate of a microorganism to a single limiting substrate concentration have long been established. In recent years, it has become apparent that, under certain conditions, the growth rate of an organism may be simultaneously limited by two or more substrates. Mathematical models of double-substrate limitation fall into two categories: interactive and noninteractive models. A discussion of both types of models is presented in both conceptual and mathematical terms. An analogous case of an enzyme which requires two different substrates to produce a single product is presented. This enzyme analog indicates that both types of double-substrate limitation models appear to be feasible under certain conditions. Based upon stoichiometry and specific growth rate-substrate concentration contour plots, a method for determining the operational conditions which will lead to double-substrate limitation is presented.     

The influence of high substrate concentrations on microbial kinetics

High substrate concentrations inhibit growth and may distort the metabolism of microorganisms. Mechanisms causing substrate inhibition are discussed and used to derive several mathematical models representative of the entire concentration range, including stimulation of growth by low substrate concentrations. These kinetic models are tested with a variety of batch culture measurements of specific growth rate and respiration rate at widely-ranging substrate concentrations. Using one of the kinetic models, equations are developed for batch, continuous, and exponential-feed reactors. Comparison of results obtained in continuous culture with results from exponential-feed culture systems is shown to offer a novel experimental method for evaluating the effect of the cell age distribution on the properties and metabolic activity of a culture.     

Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil

Although plant phosphate uptake is reduced by low soil temperature, arbuscular mycorrhizal (AM) fungi are responsible for P uptake in many plants. We investigated growth and carbon allocation of the AM fungus Glomus mosseae and a host plant (Plantago lanceolata) under reduced soil temperature. Plants were grown in compartmented microcosm units to determine the impact on both fungus and roots of a constant 2.7 °C reduction in soil temperature for 16 d. C allocation was measured using two (13)CO(2) pulse labels. Although root growth was reduced by cooling, AM colonization, growth and respiration of the extraradical mycelium (ERM) and allocation of assimilated (13)C to the ERM were all unaffected; the frequency of arbuscules increased. In contrast, root respiration and (13)C content and plant P and Zn content were all reduced by cooling. Cooling had less effect on N and K, and none on Ca and Mg content. The AM fungus G. mosseae was more able to sustain activity in cooled soil than were the roots of P. lanceolata, and so enhanced plant P content under a realistic degree of soil cooling that reduced plant growth. AM fungi may therefore be an effective means to promote plant nutrition under low soil temperatures.     

Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model

Based on short-term experiments, many plant growth models – including those used in global change research – assume that an increase in temperature stimulates plant respiration (R) more than photosynthesis (P), leading to an increase in the R/P ratio. Longer-term experiments, however, have demonstrated that R/P is relatively insensitive to growth temperature. We show that both types of temperature response may be reconciled within a simple substrate-based model of plant acclimation to temperature, in which respiration is effectively limited by the supply of carbohydrates fixed through photosynthesis. The short-term, positive temperature response of R/P reflects the transient dynamics of the nonstructural carbohydrate and protein pools; the insensitivity of R/P to temperature on longer time-scales reflects the steady-state behaviour of these pools. Thus the substrate approach may provide a basis for predicting plant respiration responses to temperature that is more robust than the current modelling paradigm based on the extrapolation of results from short-term experiments. The present model predicts that the acclimated R/P depends mainly on the internal allocation of carbohydrates to protein synthesis, a better understanding of which is therefore required to underpin the wider use of a constant R/P as an alternative modelling paradigm in global change research.     

The respiratory source of CO2

Abstract Approximately half of the carbon plants fix in photosynthesis is lost in dark respiration. The major pathways for dark respiration and their control are briefly discussed in the context of a growing plant. It is suggested that whole-plant respiration may be largely ADP-limited and that fine control of the respiratory network serves to select the respiratory substrate and to partition carbon between the numerous possible fates within the network. The striking stoichiometry between whole-plant growth and respiration is reviewed, and the relationships between substrate-limited growth and ADP-limited respiration are discussed.     

Plant growth and respiration re-visited: maintenance respiration defined - it is an emergent property of, not a separate process within, the system - and why the respiration : photosynthesis ratio is conservative

Background and Aims

Plant growth and respiration still has unresolved issues, examined here using a model. The aims of this work are to compare the model''s predictions with McCree''s observation-based respiration equation which led to the ‘growth respiration/maintenance respiration paradigm’ (GMRP) – this is required to give the model credibility; to clarify the nature of maintenance respiration (MR) using a model which does not represent MR explicitly; and to examine algebraic and numerical predictions for the respiration:photosynthesis ratio.

Methods

A two-state variable growth model is constructed, with structure and substrate, applicable on plant to ecosystem scales. Four processes are represented: photosynthesis, growth with growth respiration (GR), senescence giving a flux towards litter, and a recycling of some of this flux. There are four significant parameters: growth efficiency, rate constants for substrate utilization and structure senescence, and fraction of structure returned to the substrate pool.

Key Results

The model can simulate McCree''s data on respiration, providing an alternative interpretation to the GMRP. The model''s parameters are related to parameters used in this paradigm. MR is defined and calculated in terms of the model''s parameters in two ways: first during exponential growth at zero growth rate; and secondly at equilibrium. The approaches concur. The equilibrium respiration:photosynthesis ratio has the value of 0·4, depending only on growth efficiency and recycling fraction.

Conclusions

McCree''s equation is an approximation that the model can describe; it is mistaken to interpret his second coefficient as a maintenance requirement. An MR rate is defined and extracted algebraically from the model. MR as a specific process is not required and may be replaced with an approach from which an MR rate emerges. The model suggests that the respiration:photosynthesis ratio is conservative because it depends on two parameters only whose values are likely to be similar across ecosystems.     

The Need for Simple Dynamic Equations to Describe Plant Competition

A dynamic single-equation model for plant interaction is comparedwith the competition mechanism implicit in larger simulationmodels. When light is the limiting factor, both mechanisms canbe written in the same mathematical form containing a ‘drivingforce’ and a restriction factor. In the single-equationmodel the driving force is derived directly from the RGR ofa competition-free plant. In more comprehensive models, detailedinformation on the growth of plant organs has to be generatedby submodels. When factors other than light are limiting growth, the representationof competition in crop simulation models is complex; the single-equationmodel has the same form irrespective of which factor is limitinggrowth. It is argued that simple dynamic models should be developedfor complex processes. Plant competition, dynamic model