Sucrose and Ethylene Signaling Interact to Modulate the Circadian Clock

Haydon, Michael J.; Mielczarek, Olga; Frank, Albert R.; Román, Ángela; Webb, Alex A. R.

doi:10.1104/pp.17.00592

Cited by 84 publications

(79 citation statements)

References 63 publications

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“…C‐starvation has been reported to influence the clock via several routes including stabilization of GI (Dalchau et al, ; Haydon, Mielczarek, Frank, Román, & Webb, ) and induction of PRR7 (Haydon et al, ). SnRK1 plays a major role in C‐starvation signalling (Baena‐González, ; Nunes et al, ; Toroser, Plaut, & Huber, ; Zhang et al, ).…”

Section: Discussionmentioning

confidence: 99%

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

Flis

Mengin

Ivakov

et al. 2019

Plant Cell & Environment

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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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Section: Discussionmentioning

confidence: 99%

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

Flis

Mengin

Ivakov

et al. 2019

Plant Cell & Environment

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“…Sugar is the major outcome of photosynthesis, and recently, a link between ethylene and sugar signaling and the circadian clock was established by the finding that ethylene shortens the circadian period, depending on Suc and the circadian clock evening element GIGANTEA (GI; Haydon et al, 2017). These findings reveal that Suc affects the stability of circadian oscillator proteins and can mask the effects of ethylene on the circadian system identifying novel molecular pathways for input of sugar to the Arabidopsis circadian network.…”

Section: Snrk1 As Regulator Of Developmental Transitionsmentioning

confidence: 93%

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

et al. 2018

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The evolutionarily conserved SNF1-related protein kinase 1 (SnRK1) kinase complex is a key regulator in adjusting cellular metabolism during starvation, stress conditions, and growth-promoting conditions. Over the last two decades, extensive genetic evidence for a widespread SnRK1 signaling network has accumulated. It is now well established that SnRK1 is a central integrator of energy signaling. However, little is known about the connections between the cytoplasmic and nuclear-localized SnRK1 and plastids and mitochondria as the main energy-producing compartments in the cell. Here, we review recent findings indicating how SnRK1 affects metabolic adaptation, including plastidial and mitochondrial functions. Special emphasis is put on identified direct targets of SnRK1, which would eventually enable cross talk with organelles. In this context, a number of transcription factors (TFs) are emerging as mediators of SnRK1 signaling, potentially linking SnRK1 activity to organellar functions. Furthermore, many SnRK1 targets act in various hormonal signaling pathways, which are at least partly localized in plastids. With this review, we summarize the current knowledge on SnRK1 organelle interaction and provide ideas on the potential molecular mechanisms governing these interactions. METABOLIC REPROGRAMMING BY SNRK1 KINASE ACTIVITY UNDER DIFFERENT GROWTH AND STRESS CONDITIONSAlready under optimal growth conditions, plants need to continuously adjust their metabolic balance between autotrophic growth based on photosynthesis during the day and respiration during the night. At daytime, sugars and other metabolites are produced by photosynthesis in chloroplasts and further distributed to be used in other metabolic pathways at different cellular compartments or transported to nonphotosynthetic sink tissues. During the night, starch and sugars supply carbon equivalents for respiration, providing the necessary energy for further growth and metabolic activities. Additionally, metabolic reprogramming is required for plants to adjust their metabolism to diverse biotic and abiotic environmental stimuli. This often leads to a stop of plant growth involving a reduction in ribosomal protein synthesis, and in parallel, accumulation of protective metabolites or defense compounds. This switching of cellular energy metabolism is mediated by the activity of the evolutionarily conserved AMPK/ SNF1/SnRK1 kinase complex (Box 1; Crozet et al.,

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“…Transgenic Arabidopsis seedlings expressing a luciferase circadian reporter maintain circadian rhythms for multiple days when transferred to constant white, blue, or red light (Millar, Straume, Chory, Chua, & Kay, ). By contrast, in the absence of light, or under dim blue light (1 μmol m −2 s −1 ), circadian rhythms of luciferase bioluminescence dampened to apparent arrhythmia within 24 hr in the absence of sucrose (Haydon et al, , Jones et al, ; Figure S1). To evaluate the role of green light in circadian rhythms, plants carrying a bioluminescent circadian reporter ( CCA1::LUC2 or TOC1::LUC [Jones et al, ]) were entrained to 12:12 light:dark cycles before being transferred to 10 μmol m −2 s −1 constant green light (Figure d,e).…”

Section: Resultsmentioning

confidence: 99%

“…Exogenous sucrose has previously been used to saturate plants' circadian responses to photoassimilates (Frank et al, ; Haydon et al, ; Haydon et al, ; Philippou et al, ). Interestingly, exogenous sucrose was sufficient to mask the cry1 circadian defect under constant green light but not constant blue light (Figures c and S4b).…”

Section: Discussionmentioning

confidence: 99%

Cryptochromes integrate green light signals into the circadian system

Battle

Jones

2019

Plant Cell & Environment

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Plants are acutely sensitive of their light environment, adapting their growth habit and prioritizing developmental decisions to maximize fecundity. In addition to providing an energy source and directional information, light quality also contributes to entrainment of the circadian system, an endogenous timing mechanism that integrates endogenous and environmental signalling cues to promote growth. Whereas plants' perception of red and blue portions of the spectrum are well defined, green light sensitivity remains enigmatic. In this study, we show that low fluence rates of green light are sufficient to entrain and maintain circadian rhythms in Arabidopsis and that cryptochromes contribute to this response. Importantly, green light responses are distinguishable from low blue light‐induced phenotypes. These data suggest a distinct signalling mechanism enables entrainment of the circadian system in green light‐enriched environments, such as those found in undergrowth and in densely planted monoculture.

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Sucrose and Ethylene Signaling Interact to Modulate the Circadian Clock

Cited by 84 publications

References 63 publications

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

Cryptochromes integrate green light signals into the circadian system

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