Analysis of labeling kinetics, pool sizes, and concentration gradients of metabolites reveals the operation of multiple decarboxylation pathways and rapid movement of carbon between the Calvin–Benson cycle and the CO2-concentrating shuttles in maize.
Photoperiod duration can be predicted from previous days, but irradiance fluctuates in an unpredictable manner. To investigate how allocation to starch responds to changes in these two environmental variables, Arabidopsis Col-0 was grown in a 6 h and a 12 h photoperiod at three different irradiances. The absolute rate of starch accumulation increased when photoperiod duration was shortened and when irradiance was increased. The proportion of photosynthate allocated to starch increased strongly when photoperiod duration was decreased but only slightly when irradiance was decreased. There was a small increase in the daytime level of sucrose and twofold increases in glucose, fructose and glucose 6-phosphate at a given irradiance in short photoperiods compared to long photoperiods. The rate of starch accumulation correlated strongly with sucrose and glucose levels in the light, irrespective of whether these sugars were responding to a change in photoperiod or irradiance. Whole plant carbon budget modelling revealed a selective restriction of growth in the light period in short photoperiods. It is proposed that photoperiod sensing, possibly related to the duration of the night, restricts growth in the light period in short photoperiods, increasing allocation to starch and providing more carbon reserves to support metabolism and growth in the long night.
The carbon and nitrogen metabolism of Arabidopsis plants grown in sunlight differs from plants grown with artificial light, even when the spectral quality and sinusoidal profile of sunlight are approximated experimentally.
Significance
Plants respond to environmental change by triggering biochemical and developmental networks across multiple scales. Multiscale models that link genetic input to the whole-plant scale and beyond might therefore improve biological understanding and yield prediction. We report a modular approach to build such models, validated by a framework model of
Arabidopsis thaliana
comprising four existing mathematical models. Our model brings together gene dynamics, carbon partitioning, organ growth, shoot architecture, and development in response to environmental signals. It predicted the biomass of each leaf in independent data, demonstrated flexible control of photosynthesis across photoperiods, and predicted the pleiotropic phenotype of a developmentally misregulated transgenic line. Systems biology, crop science, and ecology might thus be linked productively in a community-based approach to modeling.
Our understanding of the complex, transcriptional feedback loops in the circadian clock mechanism has depended upon quantitative, timeseries data from disparate sources. We measure clock gene RNA profiles in Arabidopsis thaliana seedlings, grown with or without exogenous sucrose, or in soil-grown plants and in wild-type and mutant backgrounds. The RNA profiles were strikingly robust across the experimental conditions, so current mathematical models are likely to be broadly applicable in leaf tissue. In addition to providing reference data, unexpected behaviours included co-expression of PRR9 and ELF4, and regulation of PRR5 by GI. Absolute RNA quantification revealed low levels of PRR9 transcripts (peak approx. 50 copies cell−1) compared with other clock genes, and threefold higher levels of LHY RNA (more than 1500 copies cell−1) than of its close relative CCA1. The data are disseminated from BioDare, an online repository for focused timeseries data, which is expected to benefit mechanistic modelling. One data subset successfully constrained clock gene expression in a complex model, using publicly available software on parallel computers, without expert tuning or programming. We outline the empirical and mathematical justification for data aggregation in understanding highly interconnected, dynamic networks such as the clock, and the observed design constraints on the resources required to make this approach widely accessible.
Diel starch turnover responds rapidly to changes in the light regime. We investigated if these responses require changes in the temporal dynamics of the circadian clock. Arabidopsis (Arabidopsis thaliana) was grown in a 12-h photoperiod for 19 d, shifted to three different reduced light levels or to low CO 2 for one light period, and returned to growth conditions. The treatments produced widespread changes in clock transcript abundance. However, almost all of the changes were restricted to extreme treatments that led to carbon starvation and were small compared to the magnitude of the circadian oscillation. Changes included repression of EARLY FLOWERNG 4, slower decay of dusk components, and a slight phase delay at the next dawn, possibly due to abrogated Evening Complex function and sustained expression of PHYTOCHROME INTERACTING FACTORs and REVEILLEs during the night. Mobilization of starch in the night occurred in a linear manner and was paced to dawn, both in moderate treatments that did not alter clock transcripts and in extreme treatments that led to severe carbon starvation. We conclude that pacing of starch mobilization to dawn does not require retrograde carbon signaling to the transcriptional clock. On the following day, growth decreased, sugars rose, and starch accumulation was stimulated in low-light-treated plants compared to controls. This adaptive response was marked after moderate treatments and occurred independently of changes in the transcriptional clock. It is probably a time-delayed response to low-C signaling in the preceding 24-h cycle, possibly including changes in PHYTOCHROME INTERACTING FACTOR and REVEILLE expression.
Plants accumulate reserves in the daytime to support growth at night. Circadian regulation of diel reserve turnover was investigated by profiling starch, sugars, glucose 6-phosphate, organic acids and amino acids during a light-dark cycle and after transfer to continuous light in Arabidopsis wild-types and in mutants lacking dawn (lhy cca1), morning (prr7 prr9), dusk (toc1, gi) or evening (elf3) clock components. The metabolite time-series were integrated with published time-series for circadian clock transcripts to identify circadian outputs that regulate central metabolism. i) Starch accumulation was slower in elf3 and prr7 prr9. It is proposed that ELF3 positively regulates starch accumulation. ii) Reducing sugars were high early in the T-cycle in elf3, revealing that ELF3 negatively regulates sucrose recycling. iii) The pattern of starch mobilization was modified in all five mutants. A model is proposed in which dawn and dusk/evening components interact to pace degradation to anticipated dawn. iv) An endogenous oscillation of glucose 6-phosphate revealed that the clock buffers metabolism against the large influx of carbon from photosynthesis. v) Low levels of organic and amino acids in lhy cca1 and high levels in prr7 prr9 provide evidence that the dawn components positively regulate the accumulation of amino acid reserves.
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