Abstract
The circadian clock is an endogenous timing system based on the self-sustained oscillation in individual cells. These cellular circadian clocks compose a multicellular circadian system working at respective levels of tissue, organ, plant body. However, how numerous cellular clocks are coordinated within a plant has been unclear. There was little information about behavior of circadian clocks at a single-cell level due to the difficulties in monitoring circadian rhythms of individual cells in an intact plant. We developed a single-cell bioluminescence imaging system using duckweed as the plant material and succeeded in observing behavior of cellular clocks in intact plants for over a week. This imaging technique quantitatively revealed heterogeneous and independent manners of cellular clock behaviors. Furthermore, these quantitative analyses uncovered the local synchronization of cellular circadian rhythms that implied phase-attractive interactions between cellular clocks. The cell-to-cell interaction looked to be too weak to coordinate cellular clocks against their heterogeneity under constant conditions. On the other hand, under light–dark conditions, the heterogeneity of cellular clocks seemed to be corrected by cell-to-cell interactions so that cellular clocks showed a clear spatial pattern of phases at a whole plant level. Thus, it was suggested that the interactions between cellular clocks was an adaptive trait working under day–night cycles to coordinate cellular clocks in a plant body. These findings provide a novel perspective for understanding spatio-temporal architectures in the plant circadian system.
Similar content being viewed by others
References
Alabadí D, Oyama T, Yanovsky MJ et al (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
Bünning E (1935) Zur Kenntnis der erblichen Tagesperiodizität bei Primärblättern von Phaseolus multiflorus. Jahrb Wissenschaftliche Bot 81:411–418
Endo M (2016) Tissue-specific circadian clocks in plants. Curr Opin Plant Biol 29:44–49
Endo M, Shimizu H, Nohales MA et al (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422
Fukuda H, Nakamichi N, Hisatsune M et al (2007) Synchronization of plant circadian oscillators with a phase delay effect of the vein network. Phys Rev Lett 99:98102
Fukuda H, Ukai K, Oyama T (2012) Self-arrangement of cellular circadian rhythms through phase-resetting in plant roots. Phys Rev E 86:41917
Gonze D, Halloy J, Goldbeter A (2002) Robustness of circadian rhythms with respect to molecular noise. Proc Natl Acad Sci USA 99:673–678
Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610
Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377
Haydon MJ, Mielczarek O, Robertson FC et al (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692
Hillman WS (1961) The Lemnaceae, or duckweeds: a review of the descriptive and experimental literature. Bot Rev 27:221–287
Hillman WS (1970) Carbon dioxide output as an index of circadian timing in Lemna photoperiodism. Plant Physiol 45:273–279
Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249
James AB, Monreal JA, Nimmo GA et al (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835
Johnson CH, Elliott JA, Foster R (2003) Entrainment of circadian programs. Chronobiol Int 20:741–774
Kawase T, Sugano SS, Shimada T, Hara-Nishimura I (2015) A direction-selective local-thresholding method, DSLT, in combination with a dye-based method for automated three-dimensional segmentation of cells and airspaces in developing leaves. Plant J 81:357–366
Kim J, Somers DE (2010) Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant Physiol 154:611–621
Kondo T, Tsudzuki T (1978) Rhythm in potassium uptake by a duckweed, Lemna gibba G3. Plant Cell Physiol 19:1465–1473
Kusakina J, Gould PD, Hall A (2014) A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant Cell Environ 37:327–340
Leise TL, Wang CW, Gitis PJ, Welsh DK (2012) Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence. PLoS One 7:e33334
Linde A-M, Eklund DM, Kubota A et al (2017) Early evolution of the land plant circadian clock. New Phytol 17:569–590
McClung CR (2013) Beyond Arabidopsis: the circadian clock in non-model plant species. Semin Cell Dev Biol 24:430–436
McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–720
Michael TP, Salomé PA, Yu HJ et al (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053
Millar AJ, Short SR, Chua NH, Kay SA (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell 4:1075–1087
Millar AJ, Carré IA, Strayer CA et al (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267:1161–1163
Miwa K, Serikawa M, Suzuki S et al (2006) Conserved expression profiles of circadian clock-related genes in two Lemna species showing long-day and short-day photoperiodic flowering responses. Plant Cell Physiol 47:601–612
Miyata H, Yamamoto Y (1969) Rhythms in respiratory metabolism of Lemna gibba G3 under continuous illumination. Plant Cell Physiol 10:875–889
Muranaka T, Oyama T (2016) Heterogeneity of cellular circadian clocks in intact plants and its correction under light-dark cycles. Sci Adv 2:e1600500
Muranaka T, Kubota S, Oyama T (2013) A single-cell bioluminescence imaging system for monitoring cellular gene expression in a plant body. Plant Cell Physiol 54:2085–2093
Muranaka T, Okada M, Yomo J et al (2015) Characterisation of circadian rhythms of various duckweeds. Plant Biol 17:66–74
Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22:R648–R657
Nakamichi N, Ito S, Oyama T et al (2004) Characterization of plant circadian rhythms by employing Arabidopsis cultured cells with bioluminescence reporters. Plant Cell Physiol 45:57–67
Nohales MA, Kay SA (2016) Molecular mechanisms at the core of the plant circadian oscillator. Nat Struct Mol Biol 23:1061–106
Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161
Okada R, Kondo S, Satbhai SB et al (2009) Functional characterization of CCA1/LHY homolog genes, PpCCA1a and PpCCA1b, in the moss Physcomitrella patens. Plant J 60:551–563
Okada M, Muranaka T, Ito S, Oyama T (2017) Synchrony of plant cellular circadian clocks with heterogeneous properties under light/dark cycles. Sci Rep 7:317
Park DH, Somers DE, Kim YS et al (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285:1579–1582
Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 25:159–184
Plautz JD, Straume M, Stanewsky R et al (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythm 12:204–217
Seo PJ, Más P (2014) Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant Cell 26:79–87
Serikawa M, Miwa K, Kondo T, Oyama T (2008) Functional conservation of clock-related genes in flowering plants: overexpression and RNA interference analyses of the circadian rhythm in the monocotyledon Lemna gibba. Plant Physiol 146:1952–1963
Takahashi N, Hirata Y, Aihara K, Más P (2015) A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system. Cell 163:148–159
Thain SC, Hall A, Millar AJ (2000) Functional independence of circadian clocks that regulate plant gene expression. Curr Biol 10:951–956
Thain SC, Murtas G, Lynn JR et al (2002) The circadian clock that controls gene expression in Arabidopsis is tissue specific. Plant Physiol 130:102–110
Wenden B, Toner DLK, Hodge SK et al (2012) Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc Natl Acad Sci USA 109:6757–6762
Yakir E, Hassidim M, Melamed-Book N et al (2011) Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J 68:520–531
Zielinski T, Moore AM, Troup E et al (2014) Strengths and limitations of period estimation methods for circadian data. PLoS One 9:e96462
Acknowledgements
We thank Drs. Yuki Kondo and Shigeo Sugano for their kind invitation to this special issue. We also thank for Drs. Shogo Ito and Masaaki Okada for fruitful discussions . This work was supported in part by the Japan Society for the Promotion of Science KAKENHI [Grant numbers 23657033 (T.O.), 25650098 (T.O.), 17KT0022 (T.O.), and 24-1530 (T.M.)], Iwatani Naoji Foundation (T.O.), Japan Science and Technology Agency (JST) ALCA (T.O.), and JST PRESTO (T.O.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Muranaka, T., Oyama, T. Monitoring circadian rhythms of individual cells in plants. J Plant Res 131, 15–21 (2018). https://doi.org/10.1007/s10265-017-1001-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-017-1001-x