Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when <i>Arabidopsis</i> is grown in very short photoperiods

Gibon, Yves; Pyl, Eva-Theresa; Sulpice, Ronan; Lunn, John E.; Höhne, Melanie; Günther, Manuela; Stitt, Mark

doi:10.1111/j.1365-3040.2009.01965.x

Cited by 307 publications

(321 citation statements)

References 61 publications

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“…The majority of the accessions come from Eurasia, together with some accessions from North America and Africa and derive from a range of growth habitats 35,36 . They were grown in a 8 h light/16 h dark photoperiod and high N supply in which growth was limited by C (LiC) 37 and in a 12 h light/12 h dark photoperiod at two levels of N fertilization, one allowing close to maximal growth (OpN) and another in which N limited the growth (LiN) 38 . The levels of 48 metabolites and the activities of eight enzymes in central metabolism were profiled to provide a metabolic phenotype in each growth condition (Supplementary Methods).…”

Section: Resultsmentioning

confidence: 99%

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

et al. 2014

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Growth often involves a trade-off between the performance of contending tasks; metabolic plasticity can play an important role. Here we grow 97 Arabidopsis thaliana accessions in three conditions with a differing supply of carbon and nitrogen and identify a trade-off between two tasks required for rosette growth: increasing the physical size and increasing the protein concentration. We employ the Pareto performance frontier concept to rank accessions based on their multitask performance; only a few accessions achieve a good trade-off under all three growth conditions. We determine metabolic efficiency in each accession and condition by using metabolite levels and activities of enzymes involved in growth and protein synthesis. We demonstrate that accessions with high metabolic efficiency lie closer to the performance frontier and show increased metabolic plasticity. We illustrate how public domain data can be used to search for additional contending tasks, which may underlie the sub-optimality in some accessions. L iving organisms perform many different and sometimes contending tasks, leading to trade-offs in which optimal performance of one task comes at the cost of a sub-optimal performance of another task. Trade-offs are influenced by the environment and their resolution depends on metabolic resources and plasticity 1,2 . One important environmental variable affecting plant growth is resource availability 3-6 . We first ask whether there is a trade-off between two tasks during vegetative growth of Arabidopsis thaliana: the maximization of physical size and the maximization of protein concentration. We then apply two methods to rank accessions: the first based solely on the performance of tasks, and the second based on the efficiency with which metabolic resources are deployed to perform tasks. In addition, we investigate whether the trade-off and the ranking of accessions are affected by the availability of carbon (C) and nitrogen (N) and the way in which it shapes the accession-specific metabolic profiles.Plants use light energy to transform CO 2 and inorganic nutrients into a plethora of metabolic precursors that are used to drive growth. As plants are sessile, resource acquisition is constrained by their physical size. In land plants, the majority of a mature cell is occupied by the vacuole, allowing the generation of a much larger physical size per unit protein than is usually obtained by microbes or animals 7 . For simplification, we do not consider the impact of shape and phenology on the relation between physical size and resource acquisition. On the other hand, proteins are required to catalyse the transformation of resources into biomass. In particular, the majority of the protein in a plant leaf is involved in photosynthesis [8][9][10] . We hypothesize that there is a trade-off between physical size and protein concentration. While production of leaves with a higher protein concentration will allow higher rates of photosynthesis and metabolism per unit biomass, it also increases the costs of growth a...

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Section: Resultsmentioning

confidence: 99%

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

et al. 2014

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“…While active maintenance of carbon reserves could counteract depletion through a shift from growth to storage as suggested in some other studies (Smith and Stitt 2007; Gibon et al. 2009), this is unlikely as photosynthesis likely would not be possible at extremely low light levels, although we did not measure gas exchange directly. In the species with the lowest initial NSC.…”

Section: Discussionmentioning

confidence: 99%

Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species

Maguire

Kobe

2015

Ecology and Evolution

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Plants that store nonstructural carbohydrates (NSC) may rely on carbon reserves to survive carbon‐limiting stress, assuming that reserves can be mobilized. We asked whether carbon reserves decrease in resource stressed seedlings, and if NSC allocation is related to species' relative stress tolerances. We tested the effects of stress (shade, drought, and defoliation) on NSC in seedlings of five temperate tree species (Acer rubrum Marsh., Betula papyrifera Marsh., Fraxinus americana L ., Quercus rubra L., and Quercus velutina Lam.). In a greenhouse experiment, seedlings were subjected to combinations of shade, drought, and defoliation. We harvested seedlings over 32–97 days and measured biomass and NSC concentrations in stems and roots to estimate depletion rates. For all species and treatments, except for defoliation, seedling growth and NSC accumulation ceased. Shade and drought combined caused total NSC decreases in all species. For shade or drought alone, only some species experienced decreases. Starch followed similar patterns as total NSC, but soluble sugars increased under drought for drought‐tolerant species. These results provide evidence that species deplete stored carbon in response to carbon limiting stress and that species differences in NSC response may be important for understanding carbon depletion as a buffer against shade‐ and drought‐induced mortality.

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“…Aliquots of approximately 20 mg fresh weight were extracted as in Gibon et al (2009). Assays were prepared in 96-well polystyrene microplates (Sarstedt) using a robotized platform (Hamilton).…”

Section: Extraction and Assay Of Enzymesmentioning

confidence: 99%

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

et al. 2013

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Successful completion of fruit developmental programs depends on the interplay between multiple phytohormones. However, besides ethylene, the impact of other hormones on fruit quality traits remains elusive. A previous study has shown that downregulation of SlARF4, a member of the tomato (Solanum lycopersicum) auxin response factor (ARF) gene family, results in a darkgreen fruit phenotype with increased chloroplasts (Jones et al., 2002). This study further examines the role of this auxin transcriptional regulator during tomato fruit development at the level of transcripts, enzyme activities, and metabolites. It is noteworthy that the dark-green phenotype of antisense SlARF4-suppressed lines is restricted to fruit, suggesting that SlARF4 controls chlorophyll accumulation specifically in this organ. The SlARF4 underexpressing lines accumulate more starch at early stages of fruit development and display enhanced chlorophyll content and photochemical efficiency, which is consistent with the idea that fruit photosynthetic activity accounts for the elevated starch levels. SlARF4 expression is high in pericarp tissues of immature fruit and then undergoes a dramatic decline at the onset of ripening concomitant with the increase in sugar content. The higher starch content in developing fruits of SlARF4 down-regulated lines correlates with the up-regulation of genes and enzyme activities involved in starch biosynthesis, suggesting their negative regulation by SlARF4. Altogether, the data uncover the involvement of ARFs in the control of sugar content, an essential feature of fruit quality, and provide insight into the link between auxin signaling, chloroplastic activity, and sugar metabolism in developing fruit.

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Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods

Cited by 307 publications

References 61 publications

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

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