Continuous dynamic adjustment of the plant circadian oscillator

Webb, Alex A. R.; Seki, M.; Satake, Akiko; Caldana, Camila

doi:10.1038/s41467-019-08398-5

Cited by 132 publications

(124 citation statements)

References 75 publications

Supporting

Mentioning

118

Contrasting

Unclassified

Order By: Relevance

“…The clock, in its role as master regulator, must balance these two competing requirements. Recently it has been proposed that the clock in plants is dynamically plastic, able to respond to changes in environmental inputs by altering phase and period (54,55). A decentralized structure, with organ specific inputs to clocks that are coupled together, could allow some flexibility in sensing the environment whilst ensuring robust timing.…”

Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Greenwood

Domijan

Gould

et al. 2019

Preprint

View full text Add to dashboard Cite

29Every plant cell has a genetic circuit, the circadian clock, that times key processes 30 to the day-night cycle. These clocks are aligned to the day-night cycle by multiple 31 environmental signals that vary across the plant. How does the plant integrate 32 clock rhythms, both within and between organs, to ensure coordinated timing? 33To address this question, we examined the clock at the sub-tissue level across 34Arabidopsis thaliana seedlings under multiple environmental conditions and 35 genetic backgrounds. Our results show that the clock runs at different speeds 36 (periods) in each organ, which causes the clock to peak at different times across 37 the plant in both constant environmental conditions and light-dark cycles. Closer 38 examination reveals that spatial waves of clock gene expression propagate both 39 within and between organs. Using a combination of modeling and experiment, 40we reveal that these spatial waves are the result of the period differences 41 between organs and local coupling, rather than long distance signaling. With 42 further experiments we show that the endogenous period differences, and thus 43 the spatial waves, are caused by the organ specificity of inputs into the clock. We 44 demonstrate this by modulating periods using light and metabolic signals, as 45 well as with genetic perturbations. Our results reveal that plant clocks are set 46 locally by organ specific inputs, but coordinated globally via spatial waves of 47 clock gene expression. 48 49

show abstract

Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Greenwood

Domijan

Gould

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…The clock, in its role as master regulator, must balance the competing requirements of flexibility and robustness. Recently, it has been proposed that the clock in plants is dynamically plastic, able to respond to changes in environmental inputs by altering its period and phase [77,78]. Cell-cell coupling increases the synchrony and robustness of oscillations, influencing how easy it is for clocks to entrain to the environment [79].…”

Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

et al. 2019

View full text Add to dashboard Cite

Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.PLOS Biology | https://doi.org/10.days at near-cellular resolution (Materials and methods). This reporter line was chosen because of its strong expression level and its similar spatial expression to other clock components [5].In order to observe the endogenous component of the rhythms, we first imaged seedlings under LL, having previously grown them under LD cycles (LD-to-LL; Fig 2A and Materials and methods). Under the LD-to-LL condition we observed phase differences of GI::LUC expression between organs ( Fig 2B and 2C). The cotyledon and hypocotyl peaked before the root, but the tip of the root peaked before the middle region of the root (Fig 2C, S1 Fig, and S1 Video). Furthermore, we observed a decrease in coherence between regions over time, with a range between the earliest and latest peaking region of 4.92 ± 3.79 h (mean ± standard deviation) in the first and 18.36 ± 5.67 h in the final oscillation. This is due to the emergence of period differences between all regions ( Fig 2D). The cotyledon maintained a mean period of 23.82 ± 0.60 h, whereas the hypocotyl and root ran at 25.41 ± 0.91 h and 28.04 ± 0.86 h, respectively. However, the root tip ran slightly faster than the middle of the root, with a mean period of 26.90 ± 0.45 h, demonstrating the presence of endogenous period differences across all regions. We verified that our results were not specific to the GI::LUC reporter, as we observed similar differences in periods and phases across the plant using luciferase reporters for promoter activity of the core clock genes PSEUDO-RESPONSE REGULATOR 9 (PRR9) [31], TI...

show abstract

“…The Input Pathways detect entraining cues that keep the circadian clock continuously synchronized to the environment. In plants, these cues include light, temperature, and sugar levels [6][7][8] . The Central Oscillator is a series of interlocking transcriptional-translational feedback loops that can generate 24-h rhythms independently of the environment.…”

mentioning

confidence: 99%

“…The EC is a protein complex formed by EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX) that also inhibits the expression of PRR7 and PRR9 the next morning. Other essential components of the oscillator include GIGANTEA (GI), REVEILLE8 (RVE8), and CCA1 HIKING EXPEDITION (CHE) [8][9][10][11] . The Output Pathways transduce the temporal information generated by the interaction between the Central Oscillator and the Input Pathways to a plethora of biochemical pathways.…”

mentioning

confidence: 99%

Rhythms of Transcription in Field-Grown Sugarcane Are Highly Organ Specific

Dantas

Almeida-Jesus

Lima

et al. 2020

Sci Rep

View full text Add to dashboard Cite

Circadian clocks improve plant fitness in a rhythmic environment. As each cell has its own circadian clock, we hypothesized that sets of cells with different functions would have distinct rhythmic behaviour. To test this, we investigated whether different organs in field-grown sugarcane follow the same rhythms in transcription. We assayed the transcriptomes of three organs during a day: leaf, a source organ; internodes 1 and 2, sink organs focused on cell division and elongation; and internode 5, a sink organ focused on sucrose storage. The leaf had twice as many rhythmic transcripts (>68%) as internodes, and the rhythmic transcriptomes of the internodes were more like each other than to those of the leaves. Among the transcripts expressed in all organs, only 7.4% showed the same rhythmic pattern. Surprisingly, the central oscillators of these organs -the networks that generate circadian rhythms -had similar dynamics, albeit with different amplitudes. The differences in rhythmic transcriptomes probably arise from amplitude differences in tissue-specific circadian clocks and different sensitivities to environmental cues, highlighted by the sampling under field conditions. The vast differences suggest that we must study tissue-specific circadian clocks in order to understand how the circadian clock increases the fitness of the whole plant.

show abstract

Continuous dynamic adjustment of the plant circadian oscillator

Cited by 132 publications

References 75 publications

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Rhythms of Transcription in Field-Grown Sugarcane Are Highly Organ Specific

Contact Info

Product

Resources

About