Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

Seki, Naoki; Tanigaki, Yusuke; Yoshida, A.; Fukuda, Hirokazu

doi:10.2525/ecb.56.93

Cited by 3 publications

(4 citation statements)

References 27 publications

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“…Interestingly, in the root, the model predicted a complex spatial pattern, with multiple phase clusters and spatial waves in a single seedling (Fig 5C and S4 Video). These patterns of gene expression were similar to the zig-zag patterns previously reported by others when roots are grown on sucrose supplemented media (16,24,35). We found that these zig-zag patterns emerged with, but not without, local coupling (S5A and S5B Fig).…”

Section: Resultssupporting

confidence: 89%

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

Greenwood

Domijan

Gould

et al. 2019

Preprint

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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

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Section: Resultssupporting

confidence: 89%

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

“…Interestingly, in the root, the model predicted a complex spatial pattern, with multiple phase clusters and spatial waves in a single seedling ( Fig 5C and S4 Video). These patterns of gene expression were similar to the zigzag patterns previously reported by others, when roots are grown on Coordination of circadian timing in A. thaliana sucrose supplemented media [20,27,46]. We found that these zigzag patterns emerged with, but not without, local coupling (S10 Fig).…”

Section: Local Coupling Limits Desynchrony In the Absence Of Entrainmentsupporting

confidence: 89%

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

et al. 2019

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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...

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“…In the current study, the size of one pixel in the image is about 230 μm, and time-series data at a certain height are the average of several pixels. The size of cells in the Arabidopsis root is about 10 to 100 μm; therefore, one time-series is the sum of at least 100 cells (Seki et al, 2018). Moreover, phase-dependent response of amplitudes were also observed (Suppl.…”

Section: Resultsmentioning

confidence: 99%

“…The root circadian clock was reset to subjective dusk at the root tip (Fukuda et al, 2012; Voß et al, 2015). Thus, the pattern of secondary root generation may also be related to the spatiotemporal pattern of the circadian clock in plant roots (Seki et al, 2018). Several studies have reported differences in entrainment properties depending on the clock genes (Michael et al, 2003a; Flis et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Unstable Phase Response Curves Shown by Spatiotemporal Patterns in the Plant Root Circadian Clock

Masuda

Fukuda

2021

J Biol Rhythms

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Phase response curves (PRCs) play important roles in the entrainment of periodic environmental cycles. Measuring the PRC is necessary to elucidate the relationship between environmental cues and the circadian clock. Conversely, the PRCs of plant circadian clocks are unstable due to multiple factors such as biotic/abiotic noise, individual differences, changes in amplitude, growth stage, and organ/tissue specificity. However, evaluating the effect of each factor is important because PRCs are commonly obtained by determining the response of many individuals, which include different amplitude states and organs. The plant root circadian clock spontaneously generates a spatiotemporal pattern called a stripe pattern, whereby all phases of the circadian rhythm exist within an individual root. Therefore, stimulating a plant root expressing this pattern enables phase responses at all phases to be measured using an individual root. In this study, we measured PRCs for thermal stimuli using this spatiotemporal pattern method and found that the PRC changed asymmetrically with positive and negative temperature stimuli. Individual differences were observed for weak but not for strong temperature stimuli. The root PRC changed depending on the amplitude of the circadian rhythm. The PRC in the young root near the hypocotyl was more sensitive than those in older roots or near the tip. Simulation with a phase oscillator model revealed the effect of measurement and internal noises on the PRC. These results indicate that instability in the entrainment of the plant circadian clock involves multiple factors, each having different characteristics. These results may help us understand how plant circadian clocks adapt to unstable environments and how plant circadian clocks with different characteristics, such as organ, age, and amplitude, are integrated within individuals.

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Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

Cited by 3 publications

References 27 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

Unstable Phase Response Curves Shown by Spatiotemporal Patterns in the Plant Root Circadian Clock

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