Heterogeneity of cellular circadian clocks in intact plants and its correction under light-dark cycles

Muranaka, Tomoaki; Oyama, Tokitaka

doi:10.1126/sciadv.1600500

Cited by 69 publications

(130 citation statements)

References 33 publications

(61 reference statements)

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“…As discussed in this article, recent work demonstrated that the expression patterns of the clock genes show tissue-specific variations in Arabidopsis, and that the clock in each specific tissue differently affects each specific output, as it was shown that the functional vascular clock is essential for controlling photoperiodic flowering (Endo et al, 2014;Shimizu et al, 2015). As was also shown recently, the plant clock in each cell can synchronize within and across the tissues (Wenden et al, 2012;Takahashi et al, 2015;Muranaka and Oyama, 2016), although they can independently sustain circadian rhythmicity in clock gene transcription. Similar to the synchronization of the clock-regulated genes observed, do the phloem companion cells that express FT also communicate with each other to coordinate the timing of expression of FT?…”

Section: Future Perspectivesmentioning

confidence: 60%

“…Previous reports showed that a local cell-to-cell rhythm coupling mechanism exists, and it creates spatiotemporal waves of clock gene expression especially under constant light conditions (Fukuda et al, 2007;Wenden et al, 2012). Local coupling of rhythms among neighboring cells is also observed in duckweed cells, but light signal overwrites local coupling effect and masks heterogeneity of individual cell rhythmicity (Muranaka and Oyama, 2016). The Arabidopsis clock in the shoot Figure 1.…”

Section: Tissue Specificity In Clock Functionmentioning

confidence: 96%

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Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

2016

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Plants sense changes in day length (= photoperiod) as a reliable seasonal cue to regulate important developmental transitions such as flowering. Integration of various external light information into the circadian clock-controlled mechanisms enables plants to precisely measure photoperiod changes in the surrounding environment. The core mechanism of photoperiodic measurement is regulation of CONSTANS (CO) activity, which takes place in phloem companion cells in leaves. Until recently, it remained unclear whether plants possess specific variations of the clock for this regulation. Now it is known that a specific circadian timing mechanism in the vascular tissue is essential for photoperiodic flowering. In addition to spatial tissue-specific regulation, temporal regulation of CO activity is also important. The identification and characterization of multiple regulators that physically interact with CO and influence its function in the morning in long days are two recent advances in photoperiodic regulation of flowering time. It seems that CO acts as a network hub to integrate various external and internal signals into the photoperiodic flowering pathway. CO regulates the amount of FLOWERING LOCUS T (FT) transcripts and FT protein moves from companion cells of leaf phloem to the shoot apical meristem. The protein that helps long-distance transport of FT protein was also identified recently. Here, we introduce recent advances in tissue-specific variations of the circadian clock and the emerging picture of the intricate connections of transcriptional regulators through CO in the morning, which all facilitate plants knowing when to flower.Properly timing the floral transition is crucial for reproductive success. It can also influence the early development of offspring. To optimize this timing, plants constantly monitor changes in the surrounding environment. Among various environmental factors, observing changes in day length (= photoperiod) is the most reliable way for many organisms to know the specific time of year. Therefore, photoperiodic regulation is one of the major flowering time mechanisms and it has been studied since it was first reported in 1920 (Song et al., 2015). Arabidopsis (Arabidopsis thaliana), as it flowers mainly in spring, can sense lengthening days to induce flowering and became a suitable model to study photoperiodic flowering regulation. (Andrés and Coupland, 2012;Song et al., 2013;Pajoro et al., 2014;Shim and Imaizumi, 2015).In principle, photoperiodic flowering mechanisms can be divided into three parts: light input, circadian clock, and output. Light information is integrated into innate photoperiodic timing mechanisms governed by the circadian clock to induce genes that trigger flowering.

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Section: Future Perspectivesmentioning

confidence: 60%

Section: Tissue Specificity In Clock Functionmentioning

confidence: 96%

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

2016

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“…1) 2 , and we assumed that individual cells in a plant body might show rhythms differently entrained in T-cycle conditions. First, the AtCCA1::LUC bioluminescence of individual cells was monitored under the following T-cycle conditions: T = 24 h, 20 h, 16 h and 12 h (upper panels in Fig.…”

Section: Resultsmentioning

confidence: 99%

Synchrony of plant cellular circadian clocks with heterogeneous properties under light/dark cycles

Okada

Muranaka

Ito

et al. 2017

Sci Rep

Self Cite

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Individual cells in a plant can work independently as circadian clocks, and their properties are the basis of various circadian phenomena. The behaviour of individual cellular clocks in Lemna gibba was orderly under 24-h light/dark cycles despite their heterogeneous free-running periods (FRPs). Here, we reveal the entrainment habits of heterogeneous cellular clocks using non-24-h light/dark cycles (T-cycles). The cellular rhythms of AtCCA1::LUC under T = 16 h cycles showed heterogeneous entrainment that was associated with their heterogeneous FRPs. Under T = 12 h cycles, most cells showed rhythms having ~24-h periods. This suggested that the lower limit of entrainment to the light/dark cycles of heterogeneous cellular circadian clocks is set to a period longer than 12 h, which enables them to be synchronous under ~24-h daily cycles without being perturbed by short light/dark cycles. The entrainment habits of individual cellular clocks are likely to be the basis of the circadian behaviour of plant under the natural day–night cycle with noisy environmental fluctuations. We further suggest that modifications of EARLY FLOWERING3 (ELF3) in individual cells deviate the entrainability to shorter T-cycles possibly by altering both the FRPs and light responsiveness.

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“…Welsh and co-workers first reported that neurons within the suprachiasmatic nucleus (SCN; the master pacemaker in the hypothalamus of mammals) are surprisingly heterogeneous in their intrinsic periods of circadian firing pattern (Welsh et al, 1995). Subsequent studies revealed that such period-heterogeneity is not restricted to the SCN alone, but is also characteristic of mammalian peripheral clock cells (Nagoshi et al, 2004;Leise et al, 2012) as well as of clock cells in Drosophila (Sabado et al, 2017) and plants (Yakir et al, 2011;Muranaka and Oyama, 2016). The ubiquity of this network feature suggests that heterogeneity may be functionally relevant for circadian clocks (Jagota et al, 2000;Schaap et al, 2003;Gonze et al, 2005;Bernar0d et al, 2007;Inagaki et al, 2007;VanderLeest et al, 2007;Gu et al, 2016Gu et al, , 2019, thus likely being a substrate for natural selection.…”

Section: Introductionmentioning

confidence: 99%

Heritable gene expression variability governs clonal heterogeneity in circadian period

Nikhil

Korge

Kramer

2019

Preprint

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11A ubiquitous feature of circadian clocks across life forms is its organization as a network of 12 coupled cellular oscillators. Individual cellular oscillators of the network often exhibit a 13 considerable degree of heterogeneity in their intrinsic periods. While the interaction of coupling 14 and heterogeneity in circadian clock networks is hypothesized to influence clock's entrainability, 15 our knowledge of mechanisms governing network heterogeneity remains elusive. In this study, 16 we aimed to explore the principles that underlie inter-cellular period variation in circadian clock 17 networks (clonal period-heterogeneity). To this end, we employed a laboratory selection 18 approach and derived a panel of 25 clonal cell populations exhibiting circadian periods ranging 19 from 22 h to 28 h. We report that while a single parent clone can produce progeny clones with a 20 wide distribution of circadian periods, heterogeneity is not entirely stochastically driven but has 21 a strong heritable component. By quantifying the expression of 20 circadian clock and clock-22 associated genes across our panel, we found that inheritance of different expression patterns in 23 at least three clock genes might govern clonal period-heterogeneity in circadian clock networks. 24 Furthermore, we provide preliminary evidence suggesting that epigenetic variation might 25 underlie such gene expression variation. 26 27 Evans et al., 2018). In this study, we aimed to explore the possible mechanisms underlying clonal-55 heterogeneity of circadian period in human circadian oscillator cells. 56 We hypothesised that clonal period-heterogeneity in mammalian cells is due to a) stochastic 57 variation (Geva-Zatorsky et al., 2006; Chang et al., 2008; Brock, Chang and Huang, 2009; Frank 58 and Rosner, 2012) and/or b) heritable variation (Dubnau and Losick, 2006; Gordon et al., 2009, 59 2013). Since the term 'stochastic' is used in the context of both non-heritable (external noise and 60 gene expression noise) as well as heritable gene expression variation (epigenetic stochasticity), 61 for the rest of this manuscript we define 'stochasticity' as any non-heritable variation (both 62 internal and external). To test the two hypothesis outlined above, we employed a laboratory 63 selection approach and derived a panel of 25 clonal cell lines (from a common ancestral/founding 64 culture) exhibiting a range of periods between 22h and 28h. We observed that the period-65 heterogeneity among progeny clones stemming from a single parent cell is not entirely stochastic 66 but has a substantial heritable component. We then measured expression of 20 clock and clock-67 associated genes in our panel and observed that variation in gene expression levels of at least 68 three clock genes (transcription factors) might underlie clonal period-heterogeneity. 69 Furthermore, we provide preliminary evidence that epigenetic variation might govern the 70 observed clonal-variation in gene expression. 71 72 73 74 75 157 period while D...

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Heterogeneity of cellular circadian clocks in intact plants and its correction under light-dark cycles

Abstract: Cellular circadian clocks in a plant work in coordination under light-dark cycles by correcting heterogeneous traits between them.

Cited by 69 publications

References 33 publications

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

Synchrony of plant cellular circadian clocks with heterogeneous properties under light/dark cycles

Heritable gene expression variability governs clonal heterogeneity in circadian period

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