ATP yield of plant respiration: potential, actual and unknown.

BACKGROUND AND AIMS: The ATP yield of plant respiration (ATP/hexose unit respired) quantitatively links active heterotrophic processes with substrate consumption. Despite its importance, plant respiratory ATP yield is uncertain. The aim here was to integrate current knowledge of cellular mechanisms with inferences required to fill knowledge gaps to generate a contemporary estimate of respiratory ATP yield and identify important unknowns. METHOD: A numerical balance sheet model combining respiratory carbon metabolism and electron transport pathways with uses of the resulting transmembrane electrochemical proton gradient was created and parameterized for healthy, non-photosynthesizing plant cells catabolizing sucrose or starch to produce cytosolic ATP. KEY RESULTS: Mechanistically, the number of c subunits in the mitochondrial ATP synthase Fo sector c-ring, which is unquantified in plants, affects ATP yield. A value of 10 was (justifiably) used in the model, in which case respiration of sucrose potentially yields about 27.5 ATP/hexose (0.5 ATP/hexose more from starch). Actual ATP yield often will be smaller than its potential due to bypasses of energy-conserving reactions in the respiratory chain, even in unstressed plants. Notably, all else being optimal, if 25 % of respiratory O2 uptake is via the alternative oxidase - a typically observed fraction - ATP yield falls 15 % below its potential. CONCLUSIONS: Plant respiratory ATP yield is smaller than often assumed (certainly less than older textbook values of 36-38 ATP/hexose) leading to underestimation of active-process substrate requirements. This hinders understanding of ecological/evolutionary trade-offs between competing active processes and assessments of crop growth gains possible through bioengineering of processes that consume ATP. Determining the plant mitochondrial ATP synthase c-ring size, the degree of any minimally required (useful) bypasses of energy-conserving reactions in the respiratory chain, and the magnitude of any 'leaks' in the inner mitochondrial membrane are key research needs.

Leaf O(2) uptake in the dark is independent of coincident CO(2) partial pressure.

Elevated CO(2), in the dark, is sometimes reported to inhibit leaf respiration, with respiration usually measured as CO(2) efflux. Oxygen uptake may be a better gauge of respiration because non-respiratory processes can affect dark CO(2) efflux in elevated CO(2). Two methods of quantifying O(2) uptake indicated that leaf respiration was unaffected by coincident CO(2) level in the dark.

A six-year study of sapling and large-tree growth and mortality responses to natural and induced variability in precipitation and throughfall.

Global climatic change may cause changes in regional precipitation that have important implications for forest growth in the southern United States. In 1993, a stand-level experiment was initiated on Walker Branch Watershed, Tennessee, to study the sensitivity of forest saplings and large trees to changes in soil water content. Soil water content was manipulated by gravity-driven transfer of precipitation throughfall from a dry treatment plot (-33%) to a wet treatment plot (+33%). A control plot was included. Each plot was 6400 m2. Measurements of stem diameter and observations of mortality were made on large trees and saplings of Acer rubrum L., Cornus florida L., Liriodendron tulipifera L., Nyssa sylvatica Marsh, Quercus alba L. and Quercus prinus L. every 2 weeks during six growing seasons. Saplings of C. florida and A. rubrum grew faster and mortality was less on the wet plot compared with the dry and control plots, through 6 years of soil water manipulation. Conversely, diameter growth of large trees was unaffected by the treatments. However, tree diameter growth averaged across treatments was affected by year-to- year changes in soil water status. Growth in wet years was as much as 2-3 times greater than in dry years. Relationships between tree growth, phenology and soil water potential were consistent among species and quantitative expressions were developed for application in models. These field growth data indicate that differences in seasonal patterns of rainfall within and between years have greater impacts on growth than percentage changes in rainfall applied to all rainfall events.

Effects of atmospheric CO(2) on longleaf pine: productivity and allocation as influenced by nitrogen and water.

Longleaf pine (Pinus palustris Mill.) seedlings were exposed to two concentrations of atmospheric CO(2) (365 or 720 micro mol mol(-1)) in combination with two N treatments (40 or 400 kg N ha(-1) year(-1)) and two irrigation treatments (target values of -0.5 or -1.5 MPa xylem pressure potential) in open-top chambers from March 1993 through November 1994. Irrigation treatments were imposed after seedling establishment (i.e., 19 weeks after planting). Seedlings were harvested at 4, 8, 12, and 20 months. Elevated CO(2) increased biomass production only in the high-N treatment, and the relative growth enhancement was greater for the root system than for the shoot system. In water-stressed trees, elevated CO(2) increased root biomass only at the final harvest. Root:shoot ratios were usually increased by both the elevated CO(2) and low-N treatments. In the elevated CO(2) treatment, water-stressed trees had a higher root:shoot ratio than well-watered trees as a result of a drought-induced increase in the proportion of plant biomass in roots. Well-watered seedlings consistently grew larger than water-stressed seedlings only in the high-N treatment. We conclude that available soil N was the controlling resource for the growth response to elevated CO(2) in this study. Although some growth enhancement was observed in water-stressed trees in the elevated CO(2) treatment, this response was contingent on available soil N.

Environmental controls on the photosynthesis and respiration of a boreal lichen woodland: a growing season of whole-ecosystem exchange measurements by eddy correlation.

Measurements of net ecosystem CO2 exchange by eddy correlation, incident photosynthetically active photon flux density (PPFD), soil temperature, air temperature, and air humidity were made in a black spruce (Picea mariana) boreal woodland near Schefferville, Quebec, Canada, from June through August 1990. Nighttime respiration was between 0.5 and 1.5 kg C ha-1 h-1, increasing with temperature. Net uptake of carbon during the day peaked at 3 kg C ha-1 h-1, and the daily net uptake over the experiment was 12 kg C ha-1 day-1. Photosynthesis dropped substantially at leaf-to-air vapor pressure deficit (VPD) greater than 7 mb, presumably as a result of stomatal closure. The response of ecosystem photosynthesis to incident PPFD was markedly non-linear, with an abrupt saturation at 600 µmol m-2 s-1. This sharp saturation reflected the geometry of the spruce canopy (isolated conical crowns), the frequently overcast conditions, and an increase in VPD coincident with high radiation. The ecosystem light-use efficiency increased markedly during overcast periods as a result of a more even distribution of light across the forest surface. A mechanistic model of forest photosynthesis, parameterized with observations of leaf density and nitrogen content from a nearby stand, provided accurate predictions of forest photosynthesis. The observations and model results indicated that ecosystem carbon balance at the site is highly sensitive to temperature, and relatively insensitive to cloudiness.

Diurnal patterns of leaf photosynthesis, conductance and water potential at the top of a lowland rain forest canopy in Cameroon: measurements from the Radeau des Cimes.

Diurnal patterns of leaf conductance, net photosynthesis and water potential of five tree species were measured at the top of the canopy in a tropical lowland rain forest in southwestern Cameroon. Access to the 40 m canopy was by a large canopy-supported raft, the Radeau des Cimes. The measurements were made under ambient conditions, but the raft altered the local energy balance at times, resulting in elevated leaf temperatures. Leaf water potential was equal to or greater than the gravitational potential at 40 m in the early morning, falling to values as low as -3.0 MPa near midday. Net photosynthesis and conductance were typically highest during midmorning, with values of about 10-12 micro mol CO(2) m(-2) s(-1) and 0.2-0.3 mol H(2)O m(-2) s(-1), respectively. Leaf conductance and net photosynthesis commonly declined through midday with occasional recovery late in the day. Photosynthesis was negatively related to leaf temperature above midday air temperature maxima. These patterns were similar to those observed in other seasonally droughted evergreen communities, such as Mediterranean-climate shrubs, and indicate that environmental factors may cause stomatal closure and limit photosynthesis in tropical rain forests during the midday period.

Scaling CO2-photosynthesis relationships from the leaf to the canopy.

Responses of individual leaves to short-term changes in CO2 partial pressure have been relatively well studied. Whole-plant and plant community responses to elevated CO2 are less well understood and scaling up from leaves to canopies will be complicated if feedbacks at the small scale differ from feedbacks at the large scale. Mathematical models of leaf, canopy, and ecosystem processes are important tools in the study of effects on plants and ecosystems of global environmental change, and in particular increasing atmospheric CO2, and might be used to scale from leaves to canopies. Models are also important in assessing effects of the biosphere on the atmosphere. Presently, multilayer and big leaf models of canopy photosynthesis and energy exchange exist. Big leaf models - which are advocated here as being applicable to the evaluation of impacts of 'global change' on the biosphere - simplify much of the underlying leaf-level physics, physiology, and biochemistry, yet can retain the important features of plant-environment interactions with respect to leaf CO2 exchange processes and are able to make useful, quantitative predictions of canopy and community responses to environmental change. The basis of some big leaf models of photosynthesis, including a new model described herein, is that photosynthetic capacity and activity are scaled vertically within a canopy (by plants themselves) to match approximately the vertical profile of PPFD. The new big leaf model combines physically based models of leaf and canopy level transport processes with a biochemically based model of CO2 assimilation. Predictions made by the model are consistent with canopy CO2 exchange measurements, although a need exists for further testing of this and other canopy physiology models with independent measurements of canopy mass and energy exchange at the time scale of 1 h or less.

CO(2) Inhibits Respiration in Leaves of Rumex crispus L.

Curly dock (Rumex crispus L.) was grown from seed in a glasshouse at an ambient CO(2) partial pressure of about 35 pascals. Apparent respiration rate (CO(2) efflux in the dark) of expanded leaves was then measured at ambient CO(2) partial pressure of 5 to 95 pascals. Calculated intercellular CO(2) partial pressure was proportional to ambient CO(2) partial pressure in these short-term experiments. The CO(2) level strongly affected apparent respiration rate: a doubling of the partial pressure of CO(2) typically inhibited respiration by 25 to 30%, whereas a decrease in CO(2) elicited a corresponding increase in respiration. These responses were readily reversible. A flexible, sensitive regulatory interaction between CO(2) (a byproduct of respiration) and some component(s) of heterotrophic metabolism is indicated.