Plants are responsive to temperature, and can distinguish differences of 1ºC. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). The mechanisms of temperature perception are however largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm temperature response, and consistent with this, we show in this background that the warm temperature transcriptome 2 becomes de-repressed at low temperatures. We have discovered phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature dependent manner.The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers, integrating temperature information over the course of the night. One Sentence Summary:The plant temperature transcriptome is controlled at night by phytochromes, acting as thermoresponsive transcriptional repressors. Main Text:Plant development is responsive to temperature, and the phenology and distribution of crops and wild plants have already altered in response to climate change (1, 2). In Arabidopsis thaliana, warm temperature-mediated elongation growth and flowering is dependent on the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR4 and 5 (PIF4 and 5) (3-6). Growth at 27ºC reduces the activity of the Evening Complex (EC) resulting in greater PIF4 transcription. The EC is a transcriptional repressor made up of the proteins EARLY FLOWERING3 (ELF3), ELF4 and LUX ARRHYTHMO (LUX) (7-9). To test if the EC is also required for hypocotyl elongation responses below 22ºC, we examined the behavior of elf3-1 and lux-4 at 12 and 17ºC. Hypocotyl elongation in elf3-1 and lux-4 is largely suppressed at lower temperatures (Fig. 1A, B), which is consistent with cold temperatures being able to suppress PIF4 overexpression phenotypes (10). Since PHYTOCHROME B (PHYB) was identified as a QTL for thermal responsiveness and PIF4 activity is regulated by phytochromes (8, 11), we investigated whether these red light receptors control hypocotyl elongation in the range 12 to 22ºC. Plants lacking phytochrome activity (12) show constitutively long hypocotyls at 12ºC and 17ºC. Thus phytochromes are essential for responding to temperature (Fig. 1C, D and Fig. S1).We used transcriptome analysis to determine whether disrupted thermomorphogenesis in phyABCDE is specific for temperature signaling or is a consequence of misregulated growth pathways. To capture diurnal variation in thermoresponsiveness, we sampled seedlings over 24 hours at 22 and 27ºC. Clustering analysis reveals 20 groups of transcripts ( Fig. 2A and Fig. S3; described in supplement). Thermomorphogenesis occurs predominantly at night and is driven by PIF4. Consistent with this, we observe PIF4 is present in cluster 20, which is more highly expressed at 27ºC during darkness. Clusters 15 and 16 represent the other major groups of 3 nighttim...
Plant development is highly responsive to ambient temperature, and this trait has been linked to the ability of plants to adapt to climate change. The mechanisms by which natural populations modulate their thermoresponsiveness are not known. To address this, we surveyed Arabidopsis accessions for variation in thermal responsiveness of elongation growth and mapped the corresponding loci. We find that the transcriptional regulator EARLY FLOWERING3 (ELF3) controls elongation growth in response to temperature. Through a combination of modeling and experiments, we show that high temperature relieves the gating of growth at night, highlighting the importance of temperature-dependent repressors of growth. ELF3 gating of transcriptional targets responds rapidly and reversibly to changes in temperature. We show that the binding of ELF3 to target promoters is temperature dependent, suggesting a mechanism where temperature directly controls ELF3 activity.
The Arabidopsis circadian clock orchestrates gene regulation across the day/night cycle. Although a multiple feedback loop circuit has been shown to generate the 24-hr rhythm, it remains unclear how robust the clock is in individual cells, or how clock timing is coordinated across the plant. Here we examine clock activity at the single cell level across Arabidopsis seedlings over several days under constant environmental conditions. Our data reveal robust single cell oscillations, albeit desynchronised. In particular, we observe two waves of clock activity; one going down, and one up the root. We also find evidence of cell-to-cell coupling of the clock, especially in the root tip. A simple model shows that cell-to-cell coupling and our measured period differences between cells can generate the observed waves. Our results reveal the spatial structure of the plant clock and suggest that unlike the centralised mammalian clock, the Arabidopsis clock has multiple coordination points.
Temperature compensation of the Arabidopsis circadian clock is shown to be mediated by the interaction of light and temperature at the level of the crytochrome photoreceptors. These findings reveal that light and temperature share common input mechanisms to the circadian network.
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
These authors contributed equally to this work. SUMMARYCircadian clocks are gene networks producing 24-h oscillations at the level of clock gene expression that are synchronized to environmental cycles via light signals. The ELONGATED HYPOCOTYL 5 (HY5) transcription factor is a signalling hub acting downstream of several photoreceptors and is a key mediator of photomorphogenesis. Here we describe a mechanism by which light quality could modulate the pace of the circadian clock through governing abundance of HY5. We show that hy5 mutants display remarkably shorter period rhythms in blue but not in red light or darkness, and blue light is more efficient than red to induce accumulation of HY5 at transcriptional and post-transcriptional levels. We demonstrate that the pattern and level of HY5 accumulation modulates its binding to specific promoter elements of the majority of clock genes, but only a few of these show altered transcription in the hy5 mutant. Mathematical modelling suggests that the direct effect of HY5 on the apparently non-responsive clock genes could be masked by feedback from the clock gene network. We conclude that the information on the ratio of blue and red components of the white light spectrum is decoded and relayed to the circadian oscillator, at least partially, by HY5.
Bifurcation theory is one of the most widely used approaches for analysis of dynamical behaviour of chemical and biochemical reaction networks. Some of the interesting qualitative behaviour that are analyzed are oscillations and bistability (a situation where a system has at least two coexisting stable equilibria). Both phenomena have been identified as central features of many biological and biochemical systems. This paper, using the theory of stoichiometric network analysis (SNA) and notions from algebraic geometry, presents sufficient conditions for a reaction network to display bifurcations associated with these phenomena. The advantage of these conditions is that they impose fewer algebraic conditions on model parameters than conditions associated with standard bifurcation theorems. To derive the new conditions, a coordinate transformation will be made that will guarantee the existence of branches of positive equilibria in the system. This is particularly useful in mathematical biology, where only positive variable values are considered to be meaningful. The first part of the paper will be an extended introduction to SNA and algebraic geometry-related methods which are used in the coordinate transformation and set up of the theorems. In the second part of the paper we will focus on the derivation of bifurcation conditions using SNA and algebraic geometry. Conditions will be derived for three bifurcations: the saddle-node bifurcation, a simple branching point, both linked to bistability, and a simple Hopf bifurcation. The latter is linked to oscillatory behaviour. The conditions derived are sufficient and they extend earlier results from stoichiometric network analysis as can be found in (Aguda and Clarke in J Chem Phys 87:3461-3470, 1987; Clarke and Jiang in J Chem Phys 99:4464-4476, 1993; Gatermann et al. in J Symb Comput 40:1361-1382, 2005). In these papers some necessary conditions for two of these bifurcations were given. A set of examples will illustrate that algebraic conditions arising from given sufficient bifurcation conditions are not more difficult to interpret nor harder to calculate than those arising from necessary bifurcation conditions. Hence an increasing amount of information is gained at no extra computational cost. The theory can also be used in a second step for a systematic bifurcation analysis of larger reaction networks.
Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.PLOS Biology | https://doi.org/10.days at near-cellular resolution (Materials and methods). This reporter line was chosen because of its strong expression level and its similar spatial expression to other clock components [5].In order to observe the endogenous component of the rhythms, we first imaged seedlings under LL, having previously grown them under LD cycles (LD-to-LL; Fig 2A and Materials and methods). Under the LD-to-LL condition we observed phase differences of GI::LUC expression between organs ( Fig 2B and 2C). The cotyledon and hypocotyl peaked before the root, but the tip of the root peaked before the middle region of the root (Fig 2C, S1 Fig, and S1 Video). Furthermore, we observed a decrease in coherence between regions over time, with a range between the earliest and latest peaking region of 4.92 ± 3.79 h (mean ± standard deviation) in the first and 18.36 ± 5.67 h in the final oscillation. This is due to the emergence of period differences between all regions ( Fig 2D). The cotyledon maintained a mean period of 23.82 ± 0.60 h, whereas the hypocotyl and root ran at 25.41 ± 0.91 h and 28.04 ± 0.86 h, respectively. However, the root tip ran slightly faster than the middle of the root, with a mean period of 26.90 ± 0.45 h, demonstrating the presence of endogenous period differences across all regions. We verified that our results were not specific to the GI::LUC reporter, as we observed similar differences in periods and phases across the plant using luciferase reporters for promoter activity of the core clock genes PSEUDO-RESPONSE REGULATOR 9 (PRR9) [31], TI...
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