Growth, Morphology and Respiratory Cost Responses to Salinity in the Mangrove Plant Rhizophora Stylosa Depend on Growth Temperature.

Mangrove plants, which have evolved to inhabit tidal flats, may adjust their physiological and morphological traits to optimize their growth in saline habitats. Furthermore, the confined distribution of mangroves within warm regions suggests that warm temperature is advantageous to their growth in saline environments. We analyzed growth, morphology and respiratory responses to moderate salinity and temperature in a mangrove species, Rhizophora stylosa. The growth of R. stylosa was accelerated in moderate salinity compared with its growth in fresh water. Under warm conditions, the increased growth is accompanied by increased specific leaf area (SLA) and specific root length. Low temperature resulted in a low relative growth rate due to a low leaf area ratio and small SLA, regardless of salinity. Salinity lowered the ratio of the amounts of alternative oxidase to cytochrome c oxidase in the mitochondrial respiratory chain in leaves. Salinity enhanced the leaf respiration rate for maintenance, but under warm conditions this enhancement was compensated by a low leaf respiration rate for growth. In contrast, salinity enhanced overall leaf respiration rates at low temperature. Our results indicate that under moderate saline conditions R. stylosa leaves require warm temperatures to grow with a high rate of resource acquisition without enhancing respiratory cost.

Mechanistic drivers of stem respiration: A modelling exercise across species and seasons.

Stem respiration (RS ) plays a crucial role in plant carbon budgets. However, its poor understanding limits our ability to model woody tissue and whole-tree respiration. A biophysical model of stem water and carbon fluxes (TReSpire) was calibrated on cedar, maple and oak trees during spring and late summer. For this, stem sap flow, water potential, diameter variation, temperature, CO2 efflux, allometry and biochemistry were monitored. Shoot photosynthesis (PN ) and nonstructural carbohydrates (NSC) were additionally measured to evaluate source-sink relations. The highest RS and stem growth was found in maple and oak during spring, both being seasonally decoupled from PN and [NSC]. Temperature largely affected maintenance respiration (RM ) in the short term, but temperature-normalized RM was highly variable on a seasonal timescale. Overall, most of the respired CO2 radially diffused to the atmosphere (>87%) while the remainder was transported upward with the transpiration stream. The modelling exercise highlights the sink-driven behaviour of RS and the significance of overall metabolic activity on nitrogen (N) allocation patterns and N-normalized respiratory costs to capture RS variability over the long term. These insights should be considered when modelling plant respiration, whose representation is currently biased towards a better understanding of leaf metabolism.

TReSpire - a biophysical TRee Stem respiration model.

Mechanistic models of plant respiration remain poorly developed, especially in stems and woody tissues where measurements of CO2 efflux do not necessarily reflect local respiratory activity. We built a process-based model of stem respiration that couples water and carbon fluxes at the organ level (TReSpire). To this end, sap flow, stem diameter variations, xylem and soil water potential, stem temperature, stem CO2 efflux and nonstructural carbohydrates were measured in a maple tree, while xylem CO2 concentration and additional stem and xylem diameter variations were monitored in an ancillary tree for model validation. TReSpire realistically described: (1) turgor pressure to differentiate growing from nongrowing metabolism; (2) maintenance expenditures in xylem and outer tissues based on Arrhenius kinetics and nitrogen content; and (3) radial CO2 diffusivity and CO2 solubility and transport in the sap solution. Collinearity issues with phloem unloading rates and sugar-starch interconversion rates suggest parallel submodelling to close the stem carbon balance. TReSpire brings a breakthrough in the modelling of stem water and carbon fluxes at a detailed (hourly) temporal resolution. TReSpire is calibrated from a sink-driven perspective, and has potential to advance our understanding on stem growth dynamics, CO2 fluxes and underlying respiratory physiology across different species and phenological stages.

Plant respiration: Controlled by photosynthesis or biomass?

Two simplifying hypotheses have been proposed for whole-plant respiration. One links respiration to photosynthesis; the other to biomass. Using a first-principles carbon balance model with a prescribed live woody biomass turnover, applied at a forest research site where multidecadal measurements are available for comparison, we show that if turnover is fast the accumulation of respiring biomass is low and respiration depends primarily on photosynthesis; while if turnover is slow the accumulation of respiring biomass is high and respiration depends primarily on biomass. But the first scenario is inconsistent with evidence for substantial carry-over of fixed carbon between years, while the second implies far too great an increase in respiration during stand development-leading to depleted carbohydrate reserves and an unrealistically high mortality risk. These two mutually incompatible hypotheses are thus both incorrect. Respiration is not linearly related either to photosynthesis or to biomass, but it is more strongly controlled by recent photosynthates (and reserve availability) than by total biomass.

Core principles which explain variation in respiration across biological scales.

Contents Summary 670 I. Introduction 671 II. Principle 1 - Plant respiration performs three distinct functions 673 III. Principle 2 - Metabolic pathway flexibility underlies plant respiratory performance 676 IV. Principle 3 - Supply and demand interact over time to set plant respiration rate 677 V. Principle 4 - Plant respiratory acclimation involves adjustments in enzyme capacities 679 VI. Principle 5 - Respiration is a complex trait that helps to define, and is impacted by, plant lifestyle strategies 680 VII. Future directions 680 Acknowledgements 682 References 682 SUMMARY: Respiration is a core biological process that has important implications for the biochemistry, physiology, and ecology of plants. The study of plant respiration is thus conducted from several different perspectives by a range of scientific disciplines with dissimilar objectives, such as metabolic engineering, crop breeding, and climate-change modelling. One aspect in common among the different objectives is a need to understand and quantify the variation in respiration across scales of biological organization. The central tenet of this review is that different perspectives on respiration can complement each other when connected. To better accommodate interdisciplinary thinking, we identify distinct mechanisms which encompass the variation in respiratory rates and functions across biological scales. The relevance of these mechanisms towards variation in plant respiration are explained in the context of five core principles: (1) respiration performs three distinct functions; (2) metabolic pathway flexibility underlies respiratory performance; (3) supply and demand interact over time to set respiration rates; (4) acclimation involves adjustments in enzyme capacities; and (5) respiration is a complex trait that helps to define, and is impacted by, plant lifestyle strategies. We argue that each perspective on respiration rests on these principles to varying degrees and that broader appreciation of how respiratory variation occurs can unite research across scales.

Drought stress and tree size determine stem CO2 efflux in a tropical forest.

CO2 efflux from stems (CO2_stem ) accounts for a substantial fraction of tropical forest gross primary productivity, but the climate sensitivity of this flux remains poorly understood. We present a study of tropical forest CO2_stem from 215 trees across wet and dry seasons, at the world's longest running tropical forest drought experiment site. We show a 27% increase in wet season CO2_stem in the droughted forest relative to a control forest. This was driven by increasing CO2_stem in trees 10-40 cm diameter. Furthermore, we show that drought increases the proportion of maintenance to growth respiration in trees > 20 cm diameter, including large increases in maintenance respiration in the largest droughted trees, > 40 cm diameter. However, we found no clear taxonomic influence on CO2_stem and were unable to accurately predict how drought sensitivity altered ecosystem scale CO2_stem , due to substantial uncertainty introduced by contrasting methods previously employed to scale CO2_stem fluxes. Our findings indicate that under future scenarios of elevated drought, increases in CO2_stem may augment carbon losses, weakening or potentially reversing the tropical forest carbon sink. However, due to substantial uncertainties in scaling CO2_stem fluxes, stand-scale future estimates of changes in stem CO2 emissions remain highly uncertain.

Daytime depression in temperature-normalised stem CO2 efflux in young poplar trees is dominated by low turgor pressure rather than by internal transport of respired CO2.

Daytime decreases in temperature-normalised stem CO2 efflux (EA_D ) are commonly ascribed to internal transport of respired CO2 (FT ) or to an attenuated respiratory activity due to lowered turgor pressure. The two are difficult to separate as they are simultaneously driven by sap flow dynamics. To achieve combined gradients in turgor pressure and FT , sap flow rates in poplar trees were manipulated through severe defoliation, severe drought, moderate defoliation and moderate drought. Turgor pressure was mechanistically modelled using measurements of sap flow, stem diameter variation, and soil and stem water potential. A mass balance approach considering internal and external CO2 fluxes was applied to estimate FT . Under well-watered control conditions, both turgor pressure and sap flow, as a proxy of FT , were reliable predictors of EA_D . After tree manipulation, only turgor pressure was a robust predictor of EA_D . Moreover, FT accounted for < 15% of EA_D . Our results suggest that daytime reductions in turgor pressure and associated constrained growth are the main cause of EA_D in young poplar trees. Turgor pressure is determined by both carbohydrate supply and water availability, and should be considered to improve our widely used but inaccurate temperature-based predictions of woody tissue respiration in global models.

Simulating forest productivity along a neotropical elevational transect: temperature variation and carbon use efficiency.

A better understanding of the mechanisms controlling the magnitude and sign of carbon components in tropical forest ecosystems is important for reliable estimation of this important regional component of the global carbon cycle. We used the JULES vegetation model to simulate all components of the carbon balance at six sites along an Andes-Amazon transect across Peru and Brazil and compared the results to published field measurements. In the upper montane zone the model predicted a lack of forest vegetation, indicating a need for better parameterization of the responses of cloud forest vegetation within the model. In the lower montane and lowland zones simulated ecosystem productivity and respiration were predicted with reasonable accuracy, although not always within the error bounds of the observations. Model-predicted carbon use efficiency in this transect surprisingly did not increase with elevation, but remained close to the 'temperate' value 0.5. Upper montane forests were predicted to allocate ~50% of carbon fixation to biomass maintenance and growth, despite available measurements showing that they only allocate ~33%. This may be explained by elevational changes in the balance between growth and maintenance respiration within the forest canopy, as controlled by both temperature- and pressure-mediated processes, which is not yet well represented in current vegetation models.

Seasonally varying relationship between stem respiration, increment and carbon allocation of Norway spruce trees.

Stem respiration is an important component of an ecosystem's carbon budget. Beside environmental factors, it depends highly on tree energy demands for stem growth. Determination of the relationship between stem growth and stem respiration would help to reveal the response of stem respiration to changing climate, which is expected to substantially affect tree growth. Common measurement of stem radial increment does not record all aspects of stem growth processes, especially those connected with cell wall thickening; therefore, the relationship between stem respiration and stem radial increment may vary depending on the wood cell growth differentiation phase. This study presents results from measurements of stem respiration and increment carried out for seven growing seasons in a young Norway spruce forest. Moreover, rates of carbon allocation to stems were modeled for these years. Stem respiration was divided into maintenance (Rm) and growth respiration (Rg) based upon the mature tissue method. There was a close relationship between Rg and daily stem radial increment (dSRI), and this relationship differed before and after dSRI seasonal maximum, which was around 19 June. Before this date, Rg increased exponentially with dSRI, while after this date logarithmically. This is a result of later maxima of Rg and its slower decrease when compared with dSRI, which is connected with energy demands for cell wall thickening. Rg reached a maxima at the end of June or in July. The maximum of carbon allocation to stem peaked in late summer, when Rg mostly tended to decrease. The overall contribution of Rg to stem CO2 efflux amounted to 46.9% for the growing period from May to September and 38.2% for the year as a whole. This study shows that further deeper analysis of in situ stem growth and stem respiration dynamics is greatly needed, especially with a focus on wood formation on a cell level.

Redesigning thiamin synthesis: Prospects and potential payoffs.

Thiamin is essential for plant growth but is short-lived in vivo and energetically very costly to produce - a combination that makes thiamin biosynthesis a prime target for improvement by redesign. Thiamin consists of thiazole and pyrimidine moieties. Its high biosynthetic cost stems from use of the suicide enzyme THI4 to form the thiazole and the near-suicide enzyme THIC to form the pyrimidine. These energetic costs lower biomass yield potential and are likely compounded by environmental stresses that destroy thiamin and hence increase the rate at which it must be made. The energy costs could be slashed by refactoring the thiamin biosynthesis pathway to eliminate the suicidal THI4 and THIC reactions. To substantiate this design concept, we first document the energetic costs of the THI4 and THIC steps in the pathway and explain how cutting these costs could substantially increase crop biomass and grain yields. We then show that a refactored pathway must produce thiamin itself rather than a stripped-down analog because the thiamin molecule cannot be simplified without losing biological activity. Lastly, we consider possible energy-efficient alternatives to the inefficient natural THI4- and THIC-mediated steps.

High soil carbon dioxide concentrations inhibit root respiration of Douglas fir.

Total and basal respiration (Rt and Rb , respectively) of intact and undisturbed roots of one-year-old Douglas fir seedlings, Pseudotsuga menziesii var. glauca [Beissn] Franco, were measured at experimentally varied soil carbon dioxide concentrations ([CO2 ]). Use of specially designed root boxes and a CO2 gas-flow compensating system designed around an infrared gas analyzer (IRGA) allowed controlled delivery of CO2 to roots and simultaneous measurements of CO2 released by roots. Root respiration rate responded to each inlet [CO2 ], independent of whether the previous concentration had been higher or lower, within two to three hours (paired t test = 0.041, P= 0.622, and n= 13). Total and basal respiration rates decreased exponentially as soil [CO2 ] rose from 130 ppm, well below atmospheric [CO2 ], to 7015 ppm, a concentration not uncommon in field soils. Analyses of variance (ANOVA) showed that the effects of soil [CO2 ] on rates of total and basal root respiration were statistically significant. Root respiration rates decreased by 4 to 5 nmol CO2 g-1 dry weight of roots s-1 for every doubling of [CO2 ] according to the following equations: ln(R1 ) (nmol CO2 g-1 s-1 ) = 5.24-0.30*ln[CO2 ] with r= 0.78, P < 0.0001, and n= 70; and ln(Rb ) (nmol CO2 g-1 s-1 ) = 6.29-0.52 * ln[CO2 ] with r= 0.82, P < 0.0001, and n= 35. The sensitivity of root respiration to [CO2 ] suggests that some previous laboratory measurements of root respiration at atmospheric [CO2 ], which is 3 to 10-fold lower than [CO2 ] in field soils, overestimated root respiration in the field. Further, the potential importance of soil [CO2 ] indicates that it should be accounted for in models of below-ground carbon budgets.

Growth and maintenance respiration for individual plants in hierarchically structured canopies of Medicago sativa and Helianthus annuus: the contribution of current and old assimilates.

• Respiratory costs of Medicago sativa and Helianthus annuus individuals growing in hierarchically structured stands in a controlled environment were analysed with regard to the daily rate of carbon (C) assimilation. • Net assimilation of new C (An , g C d-1 ) and respiration rates of new (Rnew , g C d-1 ) and old C (Rold , g C d-1 ) were assessed by 13 CO2 labelling and gas exchange measurements. • Specific respiration rate of old C (rold , g C g-1 C d-1 ) decreased exponentially with increasing shoot biomass, but was not affected by the instantaneous relative growth rate (Δwi ). The growth coefficient g (Rnew : An ) was c. 0.32. In the most severely shaded subordinate plants, g was < 0.2, but low g stimulated rold . The contribution of Rnew to total respiraton (fR, new ) and the carbon use efficiency CUE (1 - R/(An  +Rnew )) were c. 0.68 and 0.62 for Δwi  > 0.1, respectively. For Δwi  < 0.1, fR, new and CUE decreased with decreasing Δwi in both dominant and subordinate plants. • The results suggest that Rold was closely related to maintenance, whereas Rnew was primarily involved in growth.

Fine-root respiration in a loblolly pine and sweetgum forest growing in elevated CO2.

• The loss of carbon below-ground through respiration of fine roots may be modified by global change. Here we tested the hypothesis that a reduction in N concentration of tree fine-roots grown in an elevated atmospheric CO2 concentration would reduce maintenance respiration and that more energy would be used for root growth and N uptake. We partitioned total fine-root respiration (RT ) between maintenance (RM ), growth (RG ), and N uptake respiration (RN ) for loblolly pine (Pinus taeda) and sweetgum (Liquidambar styraciflua) forests exposed to elevated CO2 . • A substantial increase in fine-root production contributed to a 151% increase in RG for loblolly pine in elevated CO2 . Root specific RM for pine was 24% lower under elevated CO2 but when extrapolated to the entire forest, no treatment effect could be detected. • R G (< 10%) and RN (< 3%) were small components of RM in both forests. Maintenance respiration was the vast majority of RT , and contributed 92% and 86% of these totals at the pine and sweetgum forests, respectively. • The hypothesis was rejected because the majority of fine-root respiration was used for maintenance and was not reduced by changes in root N concentration in elevated CO2 . Because of its large contribution to RT and total soil CO2 efflux, changes in RM caused by warming may greatly alter carbon losses from forests to the atmosphere.

Woody-tissue respiration for Simarouba amara and Minquartia guianensis, two tropical wet forest trees with different growth habits.

We measured CO2 efflux from stems of two tropical wet forest trees, both found in the canopy, but with very different growth habits. The species were Simarouba amara, a fast-growing species associated with gaps in old-growth forest and abundant in secondary forest, and Minquartia guianensis, a slow-growing species tolerant of low-light conditions in old-growth forest. Per unit of bole surface, CO2 efflux averaged 1.24 µmol m-2 s-1 for Simarouba and 0.83 µmol m-2s-1 for Minquartia. CO2 efflux was highly correlated with annual wood production (r 2=0.65), but only weakly correlated with stem diameter (r 2=0.22). We also partitioned the CO2 efflux into the functional components of construction and maintenance respiration. Construction respiration was estimated from annual stem dry matter production and maintenance respiration by subtracting construction respiration from the instantaneous CO2 flux. Estimated maintenance respiration was linearly related to sapwood volume (39.6 µmol m-3s-1 at 24.6° C, r 2=0.58), with no difference in the rate for the two species. Maintenance respiration per unit of sapwood volume for these tropical wet forest trees was roughly twice that of temperate conifers. A model combining construction and maintenance respiration estimated CO2 very well for these species (r 2=0.85). For our sample, maintenance respiration was 54% of the total CO2 efflux for Simarouba and 82% for Minquartia. For our sample, sapwood volume averaged 23% of stem volume when weighted by tree size, or 40% with no size weighting. Using these fractions, and a published estimate of aboveground dry-matter production, we estimate the annual cost of woody tissue respiration for primary forest at La Selva to be 220 or 350 g C m-2 year-1, depending on the assumed sapwood volume. These costs are estimated to be less than 13% of the gross production for the forest.

Woody tissue maintenance respiration of four conifers in contrasting climates.

We estimate maintenance respiration for boles of four temperate conifers (ponderosa pine, western hemlock, red pine, and slash pine) from CO2 efflux measurements in autumn, when construction respiration is low or negligible. Maintenance respiration of stems was linearly related to sapwood volume for all species; at 10°C, respiration per unit sapwood volume ranged from 4.8 to 8.3 µmol CO2 m-3 s-1. For all sites combined, respiration increased exponentially with temperature (Q 10 =1.7, r 2=0.78). We estimate that maintenance respiration of aboveground woody tissues of these conifers consumes 52-162 g C m-2 y-1, or 5-13% of net daytime carbon assimilation annually. The fraction of annual net daytime carbon fixation used for stem maintenance respiration increased linearly with the average annual temperature of the site.

Stem respiration of ponderosa pines grown in contrasting climates: implications for global climate change.

We examined the effects of climate and allocation patterns on stem respiration in ponderosa pine (Pinus ponderosa) growing on identical substrate in the cool, moist Sierra Nevada mountains and the warm, dry, Great Basin Desert. These environments are representative of current climatic conditions and those predicted to accompany a doubling of atmospheric CO2, respectively, throughout the range of many western north American conifers. A previous study found that trees growing in the desert allocate proportionally more biomass to sapwood and less to leaf area than montane trees. We tested the hypothesis that respiration rates of sapwood are lower in desert trees than in montane trees due to reduced stem maintenance respiration (physiological acclimation) or reduced construction cost of stem tissue (structural acclimation). Maintenance respiration per unit sapwood volume at 15°C did not differ between populations (desert: 6.39 ± 1.14 SE µmol m-3 s-1, montane: 6.54 ± 1.13 SE µmol m-3 s-1, P = 0.71) and declined with increasing stem diameter (P = 0.001). The temperature coefficient of respiration (Q 10) varied seasonally within both environments (P = 0.05). Construction cost of stem sapwood was the same in both environments (desert: 1.46 ± 0.009 SE g glucose g-1 sapwood, montane: 1.48 ± 0.009 SE glucose g-1 sapwood, P = 0.14). Annual construction respiration calculated from construction cost, percent carbon and relative growth rate was greater in montane populations due to higher growth rates. These data provide no evidence of respiratory acclimation by desert trees. Estimated yearly stem maintenance respiration was greater in large desert trees than in large montane trees because of higher temperatures in the desert and because of increased allocation of biomass to sapwood. By analogy, these data suggest that under predicted increases in temperature and aridity, potential increases in aboveground carbon gain due to enhanced photosynthetic rates may be partially offset by increases in maintenance respiration in large trees growing in CO2-enriched atmospheres.

Effects of CO2 enrichment on whole-plant carbon budget of seedlings of Fagus grandifolia and Acer saccharum in low irradiance.

Carbon exchange rates (CER) and whole-plant carbon balances of beech (Fagus grandifolia) and sugar maple (Acer saccharum) were compared for seedlings grown under low irradiance to determine the effects of atmospheric CO2 enrichment on shade-tolerant seedlings of co-dominant species. Under contemporary atmospheric CO2, photosynthetic rate per unit mass of beech was lower than for sugar maple, and atmospheric CO2 enrich ment enhanced photosynthesis for beech only. Aboveground respiration per unit mass decreased with CO2 enrichment for both species while root respiration per unitmass decreased for sugar maple only. Under contemporary atmoapheric CO2, beech had lower C uptake per plant than sugar maple, while C losses per plant to nocturnal aboveground and root respiration were similar for both species. Under elevated CO2, C uptake per plant was similar for both species, indicating a significant relative increase in whole-seedling CER with CO2 enrich ment for beech but not for sugar maple. Total C loss per plant to aboveground respiration was decreased for beech only because increase in sugar maple leaf mass counterbalanced a reduction in respiration rates. Carbon loss to root respiration per plant was not changed by CO2 enrichment for either species. However, changes in maintenance respiration cost and nitrogen level suggest changes in tissue composition with elevated CO2. Beech had a greater net daily C gain with CO2 enrichment than did sugar maple in contrast to a lower one under contemporary CO2. Elevated CO2 preferentially enhances the net C balance of beech by increasing photosynthesis and reducing respiration cost. In all cases, the greatest C lost was by roots, indicating the importance of belowground biomass in net C gain. Relative growth rate estimated from biomass accumulation was not affected by CO2 enrichment for either species possibly because of slow growth under low light. This study indicates the importance of direct effects of CO2 enrichment when predicting potential change in species distribution with global climate change.