Molecular investigation of organ‐autonomous expression of Arabidopsis circadian oscillators

Abstract

The circadian pacemaker in plants is a hierarchical multioscillator system that directs and maintains a 24-hr oscillation required for organism homeostasis and environmental fitness. Molecular clockwork within individual tissues and organs acts cell autonomously, showing differences in circadian expression of core oscillators and their target genes; there are functional dominance and coupling in the complex regulatory network. However, molecular characteristics of organ-specific clocks are still unknown. Here, we showed the detached shoot and root possess dynamic circadian protein-protein interactions between clock core components, periodicity in organs exhibits a difference. The period length difference between shoot and root was not remarkable in prr7-3 and prr7-3 prr9-1 mutants. In addition, the phase transition curve indicated that shoot and root clock respond differently to the resetting cues of ambient temperature. PRR9 and PRR7 compensate circadian period between 22 C and 28 C in shoot, not in root. The circadian rhythms of PRR9 or PRR7 transcript accumulation showed no difference at 22 C and 28 C in shoot, but differences were observed in root. In summary, our results reveal the specificity of dynamic circadian protein-protein interactions in organ-autonomous clocks and the critical roles of PRR9 and PRR7 in mechanisms regulating temperature compensation in aerial shoot system. K E Y W O R D Scircadian clock, organ-specific rhythm, PRRs, spatiotemporal regulation, temperature compensation

Circadian rhythms driving a fast‐paced root clock implicate species‐specific regulation in Medicago truncatula

“…Previous studies have shown that the oscillation in the roots fell behind that in the shoots with a longer period and slower peak expression in A. thaliana (James et al, 2008;Takahashi et al, 2015;Li et al, 2020). Based on these…”

“…These two pathways are tightly coupled to modulate tissuespecific circadian rhythms, which might be necessary for the adaptation of different organs to their microenvironments. The rhythmicity pathway is regulated by the circadian clock and environmental fluctuations, and the tissue-specific pathway may be affected by protein-protein interactions, chromatin interactions, and alternative promoter usage (Yeung and Naef, 2018;Li et al, 2020). Transcription factors can modulate tissue-specific gene expression by interacting with local cofactors in different tissues and organs.…”

“…Although several studies have shown that the clock of the root tip runs faster than that of other regions of the root, the overall speed of the roots is still slower than that of the aerial organs (James et al, 2008;Gould et al, 2018). It is widely accepted that the shoots drive the rhythms in the roots, and the timing of the peaks of clock gene expression is shifted to later from the hypocotyls going down to the root in A. thaliana (James et al, 2008;Takahashi et al, 2015;Bordage et al, 2016;Gould et al, 2018;Li et al, 2020). However, our results showed an advanced phase and short period of root clock, irrespective of whether the plants were grown in sand or agar medium, implying that there may be other novel signaling pathways different from the sucrosedependent regulation mechanism in the roots.…”

“…The rhythmic oscillation of gene expression underlies the rhythm of protein abundance, metabolism and physiology (Harmer, 2009;Li et al, 2020). The fast-paced root clock is necessary for specialized needs, such as organ-specific interaction of input and output, in M. truncatula.…”

“…Several clock genes, such as A. thaliana EARLY FLOWERING 4 (AtELF4), show rhythmic expression in shoots, but are arrhythmic in roots (James et al, 2008). Distinct circadian clock systems are diverse in different cell types, such as mesophyll and epidermal cells, and organs, such as the shoot apex, shoot and root (Takahashi et al, 2015;Endo, 2016;Gould et al, 2018;Greenwood et al, 2019;Li et al, 2020). However, there is an ongoing debate about the communication pathways and coupling degree between neighboring cells or tissue clocks.…”