Traveling Waves of Circadian Gene Expression in Lettuce

Ukai, Kazuyo; Inai, Koji; Nakamichi, Norihito; Ashida, Hiroshi; Yokota, Akiho; Hendrawan, Yusuf; Murase, Haruhiko; Fukuda, Hirokazu

doi:10.2525/ecb.50.237

Cited by 15 publications

(17 citation statements)

References 21 publications

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“…Spatial waves of clock gene expression have been previously reported in plant leaves (14,15,22,23) and roots (5,16,24) under LL. However, their relation to one another, and the relevance under LD cycles remained unclear.…”

Section: Resultsmentioning

confidence: 79%

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: Resultsmentioning

confidence: 79%

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

Greenwood

Domijan

Gould

et al. 2019

Preprint

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“…In this sense, the plant circadian system has properties of both local and global connections. Moreover, due to inactive cells in the vein region, the network of circadian cells in leaves shows various patterns of phase dynamics as well as phase delays689. Taking into account such inactive regions with more detailed network topology might further improve our model.…”

Section: Discussionmentioning

confidence: 99%

“…In plant, the circadian rhythms play important roles in gene expressions, photosynthesis, growth, and many other physiological processes123. The plant circadian system is composed of a large number of self-sustained cellular oscillators that synchronize with each other to produce a strong output rhythm45678910. Desynchronization of the oscillators diminishes the output circadian rhythm, whereas their resynchronization recovers the rhythm.…”

mentioning

confidence: 99%

Controlling Circadian Rhythms by Dark-Pulse Perturbations in Arabidopsis thaliana

Fukuda

Murase

Tokuda

2013

Sci Rep

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Plant circadian systems are composed of a large number of self-sustained cellular circadian oscillators. Although the light-dark signal in the natural environment is known to be the most powerful Zeitgeber for the entrainment of cellular oscillators, its effect is too strong to control the plant rhythm into various forms of synchrony. Here, we show that the application of pulse perturbations, i.e., short-term injections of darkness under constant light, provides a novel technique for controlling the synchronized behavior of plant rhythm in Arabidopsis thaliana. By destroying the synchronized cellular activities, circadian singularity was experimentally induced. The present technique is based upon the theory of phase oscillators, which does not require prior knowledge of the detailed dynamics of the plant system but only knowledge of its phase and amplitude responses to the pulse perturbation. Our approach can be applied to diverse problems of controlling biological rhythms in living systems.

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“…For example, a reporter assay for assessing expression of clock genes using AtCCA1::LUC transgenic plants in which a clock gene, CIRCADIAN CLOCK ASSOCIATED 1 (AtCCA1), from Arabidopsis thaliana is fused to the luciferase (LUC) gene as a reporter revealed that A. thaliana and lettuce roots exhibit a striped wave pattern. That is, the locations of gene expression peaks move from the base to the tip along the root Ukai et al, 2012). These striped waves often exhibit arrhythmic regions in which no circadian oscillations occur.…”

Section: Introductionmentioning

confidence: 99%

“…Plant cells act as self-sustained oscillators, with their own circadian clocks that regulate interactions with surrounding cells. Phase waves in leaves and roots (Fukuda et al, 2007;Wenden et al, 2012;Ukai et al, 2012;Fukuda et al, 2012), differences in inherent periods between tissues (Endo et al, 2014;Takahashi et al, 2015;Bordage et al, 2016), and spatiotemporal analytical data (Fukuda et al, 2007;James et al, 2008;Wenden et al, 2012;Fukuda et al, 2013) suggest that the cellular oscillator network involves nonlinear phenomena. It was also reported that growth and developmental processes in roots exhibit marked spatiotemporal patterns, such as striped waves resulting from strong phase resetting in the elongation-differentiation (ED) region of the root tip.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

Seki

Tanigaki

Yoshida

et al. 2018

Environmental Control in Biology

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The circadian system in plants is characterized by substantial cellular oscillations over an approximately 24-h period. Interactions between cellular oscillators trigger phase resets near the root meristem, resulting in localized regions of arrhythmic expression of the clock gene CCA1. The arrhythmicity of the circadian rhythm significantly impacts physiologic processes and growth; however, the exact nature of these arrhythmic regions remains unknown. In this study, we analyzed spatiotemporal patterns in CCA1 expression in arrhythmic regions using a nondestructive imaging technique. We found that formation of root arrhythmic regions involves the emergence of small spiral waves. Near the small spiral waves, the synchrony of cellular oscillations was low. Our findings provide experimental evidence that the arrhythmias are based on desynchronization of cellular oscillators and enhance our understanding of the role of circadian phenomena in root growth.

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Traveling Waves of Circadian Gene Expression in Lettuce

Cited by 15 publications

References 21 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

Controlling Circadian Rhythms by Dark-Pulse Perturbations in Arabidopsis thaliana

Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

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