Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf

Abstract

The circadian clocks that drive daily rhythms in animals are tightly coupled among the cells of some tissues. The coupling profoundly affects cellular rhythmicity and is central to contemporary understanding of circadian physiology and behavior. In contrast, studies of the clock in plant cells have largely ignored intercellular coupling, which is reported to be very weak or absent. We used luciferase reporter gene imaging to monitor circadian rhythms in leaves of Arabidopsis thaliana plants, achieving resolution close to the cellular level. Leaves grown without environmental cycles for up to 3 wk reproducibly showed spatiotemporal waves of gene expression consistent with intercellular coupling, using several reporter genes. Within individual leaves, different regions differed in phase by up to 17 h. A broad range of patterns was observed among leaves, rather than a common spatial distribution of circadian properties. Leaves exposed to light-dark cycles always had fully synchronized rhythms, which could desynchronize rapidly. After 4 d in constant light, some leaves were as desynchronized as leaves grown without any rhythmic input. Applying light-dark cycles to such a leaf resulted in full synchronization within 2-4 d. Thus, the rhythms of all cells were coupled to external light-dark cycles far more strongly than the cellular clocks were coupled to each other. Spontaneous desynchronization under constant conditions was limited, consistent with weak intercellular coupling among heterogeneous clocks. Both the weakness of coupling and the heterogeneity among cells are relevant to interpret molecular studies and to understand the physiological functions of the plant circadian clock. intercellular signaling | coupled oscillators | systems biology | plant physiology | gene regulatory networks

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

“…Consistent with this idea, different phases of rhythmicity can be maintained within the same plant (Thain et al, 2000). 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).…”

“…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?…”

Spatiotemporal Analysis of Localized Circadian Arrhythmias in Plant Roots

“…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.…”

Long-term monitoring of bioluminescence circadian rhythms of cells in a transgenic <i>Arabidopsis</i> mesophyll protoplast culture

“…Despite the heterogeneous and unstable features of cellular clocks in the duckweed plant, partial synchronization between neighboring cells was suggested. In Arabidopsis as well, cell-to-cell interactions for synchronization of cellular clocks were suggested (Fukuda et al 2007;Wenden et al 2012). The circadian rhythms of vascular tissues were also reported to be robust and dominant over those of mesophyll tissues in Arabidopsis (Endo et al 2014).…”