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Temporal aspects of copper homeostasis and its crosstalk with hormones.

Peñarrubia L, Romero P, Carrió-Seguí A, Andrés-Bordería A, Moreno J, Sanz A - Front Plant Sci (2015)

Bottom Line: Spatial and temporal processes that can be affected by hormones include the regulation of copper uptake into roots, intracellular trafficking and compartmentalization, and long-distance transport to developing vegetative and reproductive tissues.In turn, hormone biosynthesis and signaling are also influenced by copper availability, which suggests reciprocal regulation subjected to temporal control by the central oscillator of the circadian clock.This transcriptional regulatory network, coordinates environmental and hormonal signaling with developmental pathways to allow enhanced micronutrient acquisition efficiency.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.

ABSTRACT
To cope with the dual nature of copper as being essential and toxic for cells, plants temporarily adapt the expression of copper homeostasis components to assure its delivery to cuproproteins while avoiding the interference of potential oxidative damage derived from both copper uptake and photosynthetic reactions during light hours. The circadian clock participates in the temporal organization of coordination of plant nutrition adapting metabolic responses to the daily oscillations. This timely control improves plant fitness and reproduction and holds biotechnological potential to drive increased crop yields. Hormonal pathways, including those of abscisic acid, gibberellins, ethylene, auxins, and jasmonates are also under direct clock and light control, both in mono and dicotyledons. In this review, we focus on copper transport in Arabidopsis thaliana and Oryza sativa and the presumable role of hormones in metal homeostasis matching nutrient availability to growth requirements and preventing metal toxicity. The presence of putative hormone-dependent regulatory elements in the promoters of copper transporters genes suggests hormonal regulation to match special copper requirements during plant development. Spatial and temporal processes that can be affected by hormones include the regulation of copper uptake into roots, intracellular trafficking and compartmentalization, and long-distance transport to developing vegetative and reproductive tissues. In turn, hormone biosynthesis and signaling are also influenced by copper availability, which suggests reciprocal regulation subjected to temporal control by the central oscillator of the circadian clock. This transcriptional regulatory network, coordinates environmental and hormonal signaling with developmental pathways to allow enhanced micronutrient acquisition efficiency.

No MeSH data available.


Related in: MedlinePlus

Signaling crosstalk among circadian clock, hormones and metal homeostasis. (A) Under optimal conditions (left), light signaling influences the nutritional responses in roots and signals from adequate nutrient supply are coordinated with light signaling to drive maximal coherence between roots and shoots development. Under nutrient deficiency (right), a coherence perturbation is produced. (B) The circadian clock is a key integrator of environmental processes, such as light cycles and nutrient availability, and of endogenous cycles, such as ROS oscillation and hormone metabolism. The aim of the circadian clock-mediated regulation of spatio-temporal modulators is to optimize plant growth under both optimal cycles and altered conditions. (C) Model for the effect of activators and repressors on target gene expression. The time course of mRNA accumulation from modulators’ (blue lines) target genes (red lines) under circadian control is shown throughout four daily cycles (12 h light in white and 12 h dark in gray). The circadian oscillating levels of the activator (left) and repressor (right), running in phase (upper panel) or in antiphase (lower panel) with their targets, are shown for two cycles. The dotted lines indicate lack of modulator activity. The effects on the target expression of an input (indicated by an arrow) that activates the modulator is shown during the next two cycles. The changes underwent by the mRNA levels of the target genes are modeled by the differential equation shown in the main text. The numerical integration of Eq. 1 (with auxiliary Eq. 2) was performed by the COPASI program (Hoops et al., 2006) with σ = 0 (q = 0) for time 0–2 (i.e., the first two cycles) and with σ = 0.125 (q = 1.5) from time 2 onward. The values for other constants were A = 12, α = 5.
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Figure 2: Signaling crosstalk among circadian clock, hormones and metal homeostasis. (A) Under optimal conditions (left), light signaling influences the nutritional responses in roots and signals from adequate nutrient supply are coordinated with light signaling to drive maximal coherence between roots and shoots development. Under nutrient deficiency (right), a coherence perturbation is produced. (B) The circadian clock is a key integrator of environmental processes, such as light cycles and nutrient availability, and of endogenous cycles, such as ROS oscillation and hormone metabolism. The aim of the circadian clock-mediated regulation of spatio-temporal modulators is to optimize plant growth under both optimal cycles and altered conditions. (C) Model for the effect of activators and repressors on target gene expression. The time course of mRNA accumulation from modulators’ (blue lines) target genes (red lines) under circadian control is shown throughout four daily cycles (12 h light in white and 12 h dark in gray). The circadian oscillating levels of the activator (left) and repressor (right), running in phase (upper panel) or in antiphase (lower panel) with their targets, are shown for two cycles. The dotted lines indicate lack of modulator activity. The effects on the target expression of an input (indicated by an arrow) that activates the modulator is shown during the next two cycles. The changes underwent by the mRNA levels of the target genes are modeled by the differential equation shown in the main text. The numerical integration of Eq. 1 (with auxiliary Eq. 2) was performed by the COPASI program (Hoops et al., 2006) with σ = 0 (q = 0) for time 0–2 (i.e., the first two cycles) and with σ = 0.125 (q = 1.5) from time 2 onward. The values for other constants were A = 12, α = 5.

Mentions: In this section we seek the putative spatiotemporal regulators that are the best candidates for the integration of signaling from circadian and/or light cycles, ROS, hormones and Cu homeostasis. These regulators, either activators or repressors, can respectively enhance or attenuate the gene expression of multiple target genes at different levels. Here we emphasize mainly the transcriptional and post-transcriptional regulation that contributes to temporarily adapt their functions (Figure 2).


Temporal aspects of copper homeostasis and its crosstalk with hormones.

Peñarrubia L, Romero P, Carrió-Seguí A, Andrés-Bordería A, Moreno J, Sanz A - Front Plant Sci (2015)

Signaling crosstalk among circadian clock, hormones and metal homeostasis. (A) Under optimal conditions (left), light signaling influences the nutritional responses in roots and signals from adequate nutrient supply are coordinated with light signaling to drive maximal coherence between roots and shoots development. Under nutrient deficiency (right), a coherence perturbation is produced. (B) The circadian clock is a key integrator of environmental processes, such as light cycles and nutrient availability, and of endogenous cycles, such as ROS oscillation and hormone metabolism. The aim of the circadian clock-mediated regulation of spatio-temporal modulators is to optimize plant growth under both optimal cycles and altered conditions. (C) Model for the effect of activators and repressors on target gene expression. The time course of mRNA accumulation from modulators’ (blue lines) target genes (red lines) under circadian control is shown throughout four daily cycles (12 h light in white and 12 h dark in gray). The circadian oscillating levels of the activator (left) and repressor (right), running in phase (upper panel) or in antiphase (lower panel) with their targets, are shown for two cycles. The dotted lines indicate lack of modulator activity. The effects on the target expression of an input (indicated by an arrow) that activates the modulator is shown during the next two cycles. The changes underwent by the mRNA levels of the target genes are modeled by the differential equation shown in the main text. The numerical integration of Eq. 1 (with auxiliary Eq. 2) was performed by the COPASI program (Hoops et al., 2006) with σ = 0 (q = 0) for time 0–2 (i.e., the first two cycles) and with σ = 0.125 (q = 1.5) from time 2 onward. The values for other constants were A = 12, α = 5.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 2: Signaling crosstalk among circadian clock, hormones and metal homeostasis. (A) Under optimal conditions (left), light signaling influences the nutritional responses in roots and signals from adequate nutrient supply are coordinated with light signaling to drive maximal coherence between roots and shoots development. Under nutrient deficiency (right), a coherence perturbation is produced. (B) The circadian clock is a key integrator of environmental processes, such as light cycles and nutrient availability, and of endogenous cycles, such as ROS oscillation and hormone metabolism. The aim of the circadian clock-mediated regulation of spatio-temporal modulators is to optimize plant growth under both optimal cycles and altered conditions. (C) Model for the effect of activators and repressors on target gene expression. The time course of mRNA accumulation from modulators’ (blue lines) target genes (red lines) under circadian control is shown throughout four daily cycles (12 h light in white and 12 h dark in gray). The circadian oscillating levels of the activator (left) and repressor (right), running in phase (upper panel) or in antiphase (lower panel) with their targets, are shown for two cycles. The dotted lines indicate lack of modulator activity. The effects on the target expression of an input (indicated by an arrow) that activates the modulator is shown during the next two cycles. The changes underwent by the mRNA levels of the target genes are modeled by the differential equation shown in the main text. The numerical integration of Eq. 1 (with auxiliary Eq. 2) was performed by the COPASI program (Hoops et al., 2006) with σ = 0 (q = 0) for time 0–2 (i.e., the first two cycles) and with σ = 0.125 (q = 1.5) from time 2 onward. The values for other constants were A = 12, α = 5.
Mentions: In this section we seek the putative spatiotemporal regulators that are the best candidates for the integration of signaling from circadian and/or light cycles, ROS, hormones and Cu homeostasis. These regulators, either activators or repressors, can respectively enhance or attenuate the gene expression of multiple target genes at different levels. Here we emphasize mainly the transcriptional and post-transcriptional regulation that contributes to temporarily adapt their functions (Figure 2).

Bottom Line: Spatial and temporal processes that can be affected by hormones include the regulation of copper uptake into roots, intracellular trafficking and compartmentalization, and long-distance transport to developing vegetative and reproductive tissues.In turn, hormone biosynthesis and signaling are also influenced by copper availability, which suggests reciprocal regulation subjected to temporal control by the central oscillator of the circadian clock.This transcriptional regulatory network, coordinates environmental and hormonal signaling with developmental pathways to allow enhanced micronutrient acquisition efficiency.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.

ABSTRACT
To cope with the dual nature of copper as being essential and toxic for cells, plants temporarily adapt the expression of copper homeostasis components to assure its delivery to cuproproteins while avoiding the interference of potential oxidative damage derived from both copper uptake and photosynthetic reactions during light hours. The circadian clock participates in the temporal organization of coordination of plant nutrition adapting metabolic responses to the daily oscillations. This timely control improves plant fitness and reproduction and holds biotechnological potential to drive increased crop yields. Hormonal pathways, including those of abscisic acid, gibberellins, ethylene, auxins, and jasmonates are also under direct clock and light control, both in mono and dicotyledons. In this review, we focus on copper transport in Arabidopsis thaliana and Oryza sativa and the presumable role of hormones in metal homeostasis matching nutrient availability to growth requirements and preventing metal toxicity. The presence of putative hormone-dependent regulatory elements in the promoters of copper transporters genes suggests hormonal regulation to match special copper requirements during plant development. Spatial and temporal processes that can be affected by hormones include the regulation of copper uptake into roots, intracellular trafficking and compartmentalization, and long-distance transport to developing vegetative and reproductive tissues. In turn, hormone biosynthesis and signaling are also influenced by copper availability, which suggests reciprocal regulation subjected to temporal control by the central oscillator of the circadian clock. This transcriptional regulatory network, coordinates environmental and hormonal signaling with developmental pathways to allow enhanced micronutrient acquisition efficiency.

No MeSH data available.


Related in: MedlinePlus