A meta-analysis of crop response patterns to nitrogen limitation for improved model representation.
ABSTRACT: The representation of carbon-nitrogen (N) interactions in global models of the natural or managed land surface remains an important knowledge gap. To improve global process-based models we require a better understanding of how N limitation affects photosynthesis and plant growth. Here we present the findings of a meta-analysis to quantitatively assess the impact of N limitation on source (photosynthate production) versus sink (photosynthate use) activity, based on 77 highly controlled experimental N availability studies on 11 crop species. Using meta-regressions, we find that it can be insufficient to represent N limitation in models merely as inhibiting carbon assimilation, because in crops complete N limitation more strongly influences leaf area expansion (-50%) than photosynthesis (-34%), while leaf starch is accumulating (+83%). Our analysis thus offers support for the hypothesis of sink limitation of photosynthesis and encourages the exploration of more sink-driven crop modelling approaches. We also show that leaf N concentration changes with N availability and that the allocation of N to Rubisco is reduced more strongly compared to other photosynthetic proteins at low N availability. Furthermore, our results suggest that different crop species show generally similar response patterns to N limitation, with the exception of leguminous crops, which respond differently. Our meta-analysis offers lessons for the improved depiction of N limitation in global terrestrial ecosystem models, as well as highlights knowledge gaps that need to be filled by future experimental studies on crop N limitation response.
Project description:Given the need for parallel increases in food and energy production from crops in the context of global change, crop simulation models and data sets to feed these models with photosynthesis and respiration parameters are increasingly important. This study provides information on photosynthesis and respiration for three energy crops (sunflower, kenaf, and cynara), reviews relevant information for five other crops (wheat, barley, cotton, tobacco, and grape), and assesses how conserved photosynthesis parameters are among crops. Using large data sets and optimization techniques, the C(3) leaf photosynthesis model of Farquhar, von Caemmerer, and Berry (FvCB) and an empirical night respiration model for tested energy crops accounting for effects of temperature and leaf nitrogen were parameterized. Instead of the common approach of using information on net photosynthesis response to CO(2) at the stomatal cavity (A(n)-C(i)), the model was parameterized by analysing the photosynthesis response to incident light intensity (A(n)-I(inc)). Convincing evidence is provided that the maximum Rubisco carboxylation rate or the maximum electron transport rate was very similar whether derived from A(n)-C(i) or from A(n)-I(inc) data sets. Parameters characterizing Rubisco limitation, electron transport limitation, the degree to which light inhibits leaf respiration, night respiration, and the minimum leaf nitrogen required for photosynthesis were then determined. Model predictions were validated against independent sets. Only a few FvCB parameters were conserved among crop species, thus species-specific FvCB model parameters are needed for crop modelling. Therefore, information from readily available but underexplored A(n)-I(inc) data should be re-analysed, thereby expanding the potential of combining classical photosynthetic data and the biochemical model.
Project description:Down-regulation of photosynthesis is among the most common responses observed in C<sub>3</sub> plants grown under elevated atmospheric CO<sub>2</sub> concentration ([CO<sub>2</sub>]). Down-regulation is often attributed to an insufficient capacity of sink organs to use or store the increased carbohydrate production that results from the stimulation of photosynthesis by elevated [CO<sub>2</sub>]. Down-regulation can be accentuated by inadequate nitrogen (N) supply, which may limit sink development. While there is strong evidence for down-regulation of photosynthesis at elevated [CO<sub>2</sub>] in enclosure studies most often involving potted plants, there is little evidence for this when [CO<sub>2</sub>] is elevated fully under open-air field treatment conditions. To assess the importance of sink strength on the down-regulation of photosynthesis and on the potential of N to mitigate this down-regulation under agriculturally relevant field conditions, two tobacco cultivars (<i>Nicotiana tabacum</i> L. cv. Petit Havana; cv. Mammoth) of strongly contrasting ability to produce the major sink of this crop, leaves, were grown under ambient and elevated [CO<sub>2</sub>] and with two different N additions in a free air [CO<sub>2</sub>] (FACE) facility. Photosynthetic down-regulation at elevated [CO<sub>2</sub>] reached only 9% in cv. Mammoth late in the season likely reflecting sustained sink strength of the rapidly growing plant whereas down-regulation in cv. Petit Havana reached 25%. Increased N supply partially mitigated down-regulation of photosynthesis in cv. Petit Havana and this mitigation was dependent on plant developmental stage. Overall, these field results were consistent with the hypothesis that sustained sink strength, that is the ability to utilize photosynthate, and adequate N supply will allow C<sub>3</sub> crops in the field to maintain enhanced photosynthesis and therefore productivity as [CO<sub>2</sub>] continues to rise.
Project description:In protected strawberry (Fragaria × ananassa Duch.) cultivation, environmental control based on the process of photosynthate translocation is essential for optimizing fruit quality and yield, because the process of photosynthate translocation directly affects dry matter partitioning. We visualized photosynthate translocation to strawberry fruits non-invasively with 11CO2 and a positron-emitting tracer imaging system (PETIS). We used PETIS to evaluate real-time dynamics of 11C-labeled photosynthate translocation from a 11CO2-fed leaf, which was immediately below the inflorescence, to individual fruits on an inflorescence in intact plant. Serial photosynthate translocation images and animations obtained by PETIS verified that the 11C-photosynthates from the source leaf reached the sink fruit within 1 h but did not accumulate homogeneously within a fruit. The quantity of photosynthate translocation as represented by 11C radioactivity varied among individual fruits and their positions on the inflorescence. Photosynthate translocation rates to secondary fruit were faster than those to primary or tertiary fruits, even though the translocation pathway from leaf to fruit was the longest for the secondary fruit. Moreover, the secondary fruit was 25% smaller than the primary fruit. Sink activity (11C radioactivity/dry weight [DW]) of the secondary fruit was higher than those of the primary and tertiary fruits. These relative differences in sink activity levels among the three fruit positions were also confirmed by 13C tracer measurement. Photosynthate translocation rates in the pedicels might be dependent on the sink strength of the adjoining fruits. The present study established 11C-photosynthate arrival times to the sink fruits and demonstrated that the translocated material does not uniformly accumulate within a fruit. The actual quantities of translocated photosynthates from a specific leaf differed among individual fruits on the same inflorescence. To the best of our knowledge, this is the first reported observation of real-time translocation to individual fruits in an intact strawberry plant using 11C-radioactive- and 13C-stable-isotope analyses.
Project description:Arabidopsis thaliana hybrids have similar properties to hybrid crops, with greater biomass relative to the parents. We asked whether the greater biomass was due to increased photosynthetic efficiency per unit leaf area or to overall increased leaf area and increased total photosynthate per plant. We found that photosynthetic parameters (electron transport rate, CO2 assimilation rate, chlorophyll content, and chloroplast number) were unchanged on a leaf unit area and unit fresh weight basis between parents and hybrids, indicating that heterosis is not a result of increased photosynthetic efficiency. To investigate the possibility of increased leaf area producing more photosynthate per plant, we studied C24×Landsberg erecta (Ler) hybrids in detail. These hybrids have earlier germination and leaf growth than the parents, leading to a larger leaf area at any point in development of the plant. The developing leaves of the hybrids are significantly larger than those of the parents, with consequent greater production of photosynthate and an increased contribution to heterosis. The set of leaves contributing to heterosis changes as the plant develops; the four most recently emerged leaves make the greatest contribution. As a leaf matures, its contribution to heterosis attenuates. While photosynthesis per unit leaf area is unchanged at any stage of development in the hybrid, leaf area is greater and the amount of photosynthate per plant is increased.
Project description:BACKGROUND: The production of flowers, fruits and seeds demands considerable energy and nutrients, which can limit the allocation of these resources to other plant functions and, thereby, influence survival and future reproduction. The magnitude of the physiological costs of reproduction depends on both the factors limiting seed production (pollen, ovules or resources) and the capacity of plants to compensate for high resource demand. METHODS: To assess the magnitude and consequences of reproductive costs, we used shading and defoliation to reduce photosynthate production by fully pollinated plants of a perennial legume, Oxytropis sericea (Fabaceae), and examined the resulting impact on photosynthate allocation, and nectar, fruit and seed production. KEY RESULTS: Although these leaf manipulations reduced photosynthesis and nectar production, they did not alter photosynthate allocation, as revealed by (13)C tracing, or fruit or seed production. That photosynthate allocation to reproductive organs increased >190 % and taproot mass declined by 29 % between flowering and fruiting indicates that reproduction was physiologically costly. CONCLUSIONS: The insensitivity of fruit and seed production to leaf manipulation is consistent with either compensatory mobilization of stored resources or ovule limitation. Seed production differed considerably between the two years of the study in association with contrasting precipitation prior to flowering, perhaps reflecting contrasting limits on reproductive performance.
Project description:The leaf economics spectrum (LES) is an ecophysiological concept describing the trade-offs of leaf structural and physiological traits, and has been widely investigated on multiple scales. However, the effects of the breeding process on the LES in crops, as well as the mechanisms of the trait trade-offs underlying the LES, have not been thoroughly elucidated to date. In this study, a dataset that included leaf anatomical, biochemical, and functional traits was constructed to evaluate the trait covariations and trade-offs in domesticated species, namely rice (Oryza species). The slopes and intercepts of the major bivariate correlations of the leaf traits in rice were significantly different from the global LES dataset (Glopnet), which is based on multiple non-crop species in natural ecosystems, although the general patterns were similar. The photosynthetic traits responded differently to leaf structural and biochemical changes, and mesophyll conductance was the most sensitive to leaf nitrogen (N) status. A further analysis revealed that the relative limitation of mesophyll conductance declined with leaf N content; however, the limitation of the biochemistry increased relative to leaf N content. These findings indicate that breeding selection and high-resource agricultural environments lead crops to deviate from the leaf trait covariation in wild species, and future breeding to increase the photosynthesis of rice should primarily focus on improvement of the efficiency of photosynthetic enzymes.
Project description:Interest in hemp (Cannabis sativa L.) as a crop for the biobased economy is growing worldwide because hemp produces a high and valuable biomass while requiring low inputs. To understand the physiological basis of hemp's resource-use efficiency, canopy gas exchange was assessed using a chamber technique on canopies exposed to a range of nitrogen (N) and water levels. Since canopy transpiration and carbon assimilation were very sensitive to variations in microclimate among canopy chambers, observations were adjusted for microclimatic differences using a physiological canopy model, with leaf-level parameters estimated for hemp from our previous study. Canopy photosynthetic water-use efficiency (PWUEc), defined as the ratio of gross canopy photosynthesis to canopy transpiration, ranged from 4.0 mmol CO2 (mol H2O)-1 to 7.5 mmol CO2 (mol H2O)-1. Canopy photosynthetic nitrogen-use efficiency (PNUEc), the ratio of the gross canopy photosynthesis to canopy leaf-N content, ranged from 0.3 mol CO2 d-1 (g N)-1 to 0.7 mol CO2 d-1 (g N)-1. The effect of N-input levels on PWUEc and PNUEc was largely determined by the N effect on canopy size or leaf area index (LAI), whereas the effect of water-input levels differed between short- and long-term stresses. The effect of short-term water stress was reflected by stomatal regulation. The long-term stress increased leaf senescence, decreased LAI but retained total canopy N content; however, the increased average leaf-N could not compensate for the lost LAI, leading to a decreased PNUEc. Although hemp is known as a resource-use efficient crop, its final biomass yield and nitrogen use efficiency may be restricted by water limitation during growth. Our results also suggest that crop models should take stress-induced senescence into account in addition to stomatal effects if crops experience a prolonged water stress during growth.
Project description:BACKGROUND AND AIMS: In crops other than sugarcane there is good evidence that the size and activity of carbon sinks influence source activity via sugar-related regulation of the enzymes of photosynthesis, an effect that is partly mediated through coarse regulation of gene expression. METHODS: In the current study, leaf shading treatments were used to perturb the source-sink balance in 12-month-old Saccharum spp. hybrid 'N19' (N19) by restricting source activity to a single mature leaf. Changes in leaf photosynthetic gas exchange variables and leaf and culm sugar concentrations were subsequently measured over a 14 d period. In addition, the changes in leaf gene response to the source-sink perturbation were measured by reverse northern hybridization analysis of an array of 128 expressed sequence tags (ESTs) related to photosynthetic and carbohydrate metabolism. KEY RESULTS: Sucrose concentrations in immature culm tissue declined significantly over the duration of the shading treatment, while a 57 and 88% increase in the assimilation rate (A) and electron transport rate (ETR), respectively, was observed in the source leaf. Several genes (27) in the leaf displayed a >2-fold change in expression level, including the upregulation of several genes associated with C(4) photosynthesis, mitochondrial metabolism and sugar transport. Changes in gene expression levels of several genes, including Rubisco (EC 18.104.22.168) and hexokinase (HXK; EC 22.214.171.124), correlated with changes in photosynthesis and tissue sugar concentrations that occurred subsequent to the source-sink perturbation. CONCLUSIONS: These results are consistent with the notion that sink demand may limit source activity through a kinase-mediated sugar signalling mechanism that correlates to a decrease in source hexose concentrations, which, in turn, correlate with increased expression of genes involved in photosynthesis and metabolite transport. The signal feedback system reporting sink sufficiency and regulating source activity may be a potentially valuable target for future genetic manipulation to increase sugarcane sucrose yield.
Project description:Appropriate planting density and nitrogen (N) supply are critical factors optimizing yield in crop cultivation. To advance the knowledge of maize plants under different density and N rate combinations, responses of canopy apparent photosynthesis (CAP), and assimilate redistribution characters (by 13CO2 stable isotope tracing) were investigated. In this study, two maize varieties DH618 and DH605 were grown at various planting densities (6.75, 8.25, 9.75, and 11.25 pl m-2) and N application rates (0, 180, 270, 360, and 540 kg ha-1) during 2013-2015. Maize grain yield (GY) was maximized at a density of 9.75 pl m-2 with 180-360 kg ha-1 N during the three study years. Maize GY, biomass, CAP, leaf area index (LAI), and 13C-photosynthate reallocation all responded more intensively to density than N rate, but the N response differed between varieties. We established links among CAP, LAI and biomass, and GY and kernel number per unit area (KNA). CAP depended on high LAI and enzyme activities for photosynthesis, yet both N deficiency and N excess had inhibitory effects. Besides, relations between 13C-photosynthate reallocation and yield components were executed. High density increased the 13C-photosynthate distribution in vegetative organs but reduced the allocation in ear, while N supply moderated the response. Based on our results, maize plants with greater CAP, more 13C-photosynthate distribution to ears, and less 13C-photosynthate distribution to stems under different density and N rate combinations could improve KNA and achieve a greater GY consequently.
Project description:It has been proposed that delayed leaf senescence can extend grain filling duration and thus increase yields in cereal crops. We found that wheat (Triticum aestivum) NAM RNAi plants with delayed senescence carried out 40% more flag leaf photosynthesis after anthesis than control plants, but had the same rate and duration of starch accumulation during grain filling and the same final grain weight. The additional photosynthate available in NAM RNAi plants was in part stored as fructans in the stems, whereas stem fructans were remobilised during grain filling in control plants. In both genotypes, activity of starch synthase was limiting for starch synthesis in the later stages of grain filling. We suggest that in order to realise the potential yield gains offered by delayed leaf senescence, this trait should be combined with increased grain filling capacity.