ABSTRACT
A classical question in biology is how different processes are controlled in space and time, with research pointing to different mechanisms as timers. In this collection of Voices, we asked researchers to define their scientific questions related to time-keeping and the approaches they use to answer them.
Subject(s)
Chronobiology Phenomena , Animals , Growth and DevelopmentABSTRACT
Understanding gene expression dynamics in the context of the time of day and temperature response is an important part of understanding plant thermotolerance in a changing climate. Performing "gating" experiments under constant conditions and light-dark cycles allows users to identify and dissect the contribution of the time of day and circadian clock to the dynamic nature of stress-responsive genes. Here, we describe the design of specific laboratory experiments in plants (Arabidopsis thaliana and bread wheat, Triticum aestivum) to investigate temporal responses to heat (1 h at 37 °C) or cold (3 h at 4 °C), and we include known marker genes that have circadian-gated responses to temperature changes.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Circadian Clocks , Temperature , Transcription Factors/metabolism , Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Circadian Clocks/genetics , Circadian Rhythm/genetics , Gene Expression Regulation, PlantABSTRACT
Surely most chronobiologists believe circadian clocks are an adaptation of organisms that enhances fitness, but are we certain that this focus of our research effort really confers a fitness advantage? What is the evidence, and how do we evaluate it? What are the best criteria? These questions are the topic of this review. In addition, we will discuss selective pressures that might have led to the historical evolution of circadian systems while considering the intriguing question of whether the ongoing climate change is modulating these selective pressures so that the clock is still evolving.
Subject(s)
Circadian Clocks , Circadian Clocks/genetics , Circadian RhythmABSTRACT
Diel cycles of gene expression are thought to adapt plants to 24-h changes in environmental conditions. The circadian clock contributes to this process, but less is known about circadian programs in developing reproductive organs. While model plants and controlled conditions have contributed greatly to our knowledge of circadian clock function, there is a need to better understand its role in crop plants under field conditions with fluctuating light and temperature. In this study, we investigated changes in the circadian clock during the development of grape berries of Vitis vinifera L. We found that the transcripts of circadian clock homologs had high-amplitude oscillations prior to, but not during, ripening. As ripening progressed, the amplitude and rhythmicity of the diel oscillations decreased until most transcripts tested had no significant fluctuation over the 24-h cycle. Despite this loss of rhythmicity, the majority of circadian clock genes investigated were expressed at or near their abundance at the nadir of their pre-ripening oscillation although the berries remained transcriptionally active. From this, it can be concluded that cycling of the canonical circadian clock appears unnecessary for berry ripening. Our data suggest that changes in circadian clock dynamics during reproductive organ development may have important functional consequences.
Subject(s)
Circadian Clocks , Vitis , Vitis/genetics , Vitis/metabolism , Fruit/metabolism , Circadian Clocks/genetics , Gene Expression Regulation, PlantABSTRACT
Circadian rhythms coordinate the responses of organisms with their daily fluctuating environments, by establishing a temporal program of gene expression. This schedules aspects of metabolism, physiology, development and behaviour according to the time of day. Circadian regulation in plants is extremely pervasive, and is important because it underpins both productivity and seasonal reproduction. Circadian regulation extends to the control of environmental responses through a regulatory process known as circadian gating. Circadian gating is the process whereby the circadian clock regulates the response to an environmental cue, such that the magnitude of response to an identical cue varies according to the time of day of the cue. Here, we show that there is genome-wide circadian gating of responses to cold temperatures in plants. By using bread wheat as an experimental model, we establish that circadian gating is crucial to the programs of gene expression that underlie the environmental responses of a crop of major socioeconomic importance. Furthermore, we identify that circadian gating of cold temperature responses are distributed unevenly across the three wheat subgenomes, which might reflect the geographical origins of the ancestors of modern wheat.
ABSTRACT
Circadian regulation produces a biological measure of time within cells. The daily cycle in the availability of light for photosynthesis causes dramatic changes in biochemical processes in photosynthetic organisms, with the circadian clock having crucial roles in adaptation to these fluctuating conditions. Correct alignment between the circadian clock and environmental day-night cycles maximizes plant productivity through its regulation of metabolism. Therefore, the processes that integrate circadian regulation with metabolism are key to understanding how the circadian clock contributes to plant productivity. This forms an important part of exploiting knowledge of circadian regulation to enhance sustainable crop production. Here, we examine the roles of circadian regulation in metabolic processes in source and sink organ structures of Arabidopsis. We also evaluate possible roles for circadian regulation in root exudation processes that deposit carbon into the soil, and the nature of the rhythmic interactions between plants and their associated microbial communities. Finally, we examine shared and differing aspects of the circadian regulation of metabolism between Arabidopsis and other model photosynthetic organisms, and between circadian control of metabolism in photosynthetic and non-photosynthetic organisms. This synthesis identifies a variety of future research topics, including a focus on metabolic processes that underlie biotic interactions within ecosystems.
Subject(s)
Arabidopsis , Circadian Clocks , Circadian Rhythm/physiology , Arabidopsis/metabolism , Ecosystem , Photosynthesis/physiology , Circadian Clocks/physiology , Gene Expression Regulation, PlantABSTRACT
Circadian clocks are pervasive throughout nature, yet only recently has this adaptive regulatory program been described in nonphotosynthetic bacteria. Here, we describe an inherent complexity in the Bacillus subtilis circadian clock. We find that B. subtilis entrains to blue and red light and that circadian entrainment is separable from masking through fluence titration and frequency demultiplication protocols. We identify circadian rhythmicity in constant light, consistent with the Aschoff's rule, and entrainment aftereffects, both of which are properties described for eukaryotic circadian clocks. We report that circadian rhythms occur in wild isolates of this prokaryote, thus establishing them as a general property of this species, and that its circadian system responds to the environment in a complex fashion that is consistent with multicellular eukaryotic circadian systems.
Subject(s)
Circadian Clocks , Bacillus subtilis , Circadian Rhythm , Light , EukaryotaABSTRACT
The malaria parasite Plasmodium falciparum has a nonphotosynthetic plastid called the apicoplast, which contains its own genome. Regulatory mechanisms for apicoplast gene expression remain poorly understood, despite this organelle being crucial for the parasite life cycle. Here, we identify a nuclear-encoded apicoplast RNA polymerase σ subunit (sigma factor) which, along with the α subunit, appears to mediate apicoplast transcript accumulation. This has a periodicity reminiscent of parasite circadian or developmental control. Expression of the apicoplast subunit gene, apSig, together with apicoplast transcripts, increased in the presence of the blood circadian signaling hormone melatonin. Our data suggest that the host circadian rhythm is integrated with intrinsic parasite cues to coordinate apicoplast genome transcription. This evolutionarily conserved regulatory system might be a future target for malaria treatment.
Subject(s)
Apicoplasts , Malaria , Parasites , Animals , Apicoplasts/genetics , Apicoplasts/metabolism , Parasites/genetics , Parasites/metabolism , Cues , Plasmodium falciparum/genetics , Plasmodium falciparum/metabolism , Malaria/metabolism , Protozoan Proteins/metabolismABSTRACT
Chloroplasts are a common feature of plant cells and aspects of their metabolism, including photosynthesis, are influenced by low-temperature conditions. Chloroplasts contain a small circular genome that encodes essential components of the photosynthetic apparatus and chloroplast transcription/translation machinery. Here, we show that in Arabidopsis, a nuclear-encoded sigma factor that controls chloroplast transcription (SIGMA FACTOR5) contributes to adaptation to low-temperature conditions. This process involves the regulation of SIGMA FACTOR5 expression in response to cold by the bZIP transcription factors ELONGATED HYPOCOTYL5 and ELONGATED HYPOCOTYL5 HOMOLOG. The response of this pathway to cold is gated by the circadian clock, and it enhances photosynthetic efficiency during long-term cold and freezing exposure. We identify a process that integrates low-temperature and circadian signals, and modulates the response of chloroplasts to low-temperature conditions.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Sigma Factor/genetics , Sigma Factor/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Temperature , Arabidopsis/metabolism , Photosynthesis , Gene Expression Regulation, PlantABSTRACT
Circadian clocks occur across the kingdoms of life, including some fungi and bacteria present in the root-associated soil known as the rhizosphere. Recent work from Amy Newman and colleagues, published in BMC Biology, has discovered that the circadian clock in Arabidopsis plants affects the rhythmicity of rhizosphere microbial communities This brings into play the exciting question of whether there is a bidirectional rhythmic interaction between plants and their rhizomicrobiome. Here, we discuss how the findings of Newman et al. suggest that soil microbiomes can have both self-sustained and plant-imposed rhythmicity, and the challenges of plant-microbiome circadian clock research.
Subject(s)
Arabidopsis , Circadian Clocks , Microbiota , Rhizosphere , Circadian Rhythm , Soil Microbiology , Plants/microbiology , SoilABSTRACT
The circadian clock is a finely balanced timekeeping mechanism that coordinates programmes of gene expression. It is currently unknown how the clock regulates expression of homoeologous genes in polyploids. Here, we generate a high-resolution time-course dataset to investigate the circadian balance between sets of 3 homoeologous genes (triads) from hexaploid bread wheat. We find a large proportion of circadian triads exhibit imbalanced rhythmic expression patterns, with no specific subgenome favoured. In wheat, period lengths of rhythmic transcripts are found to be longer and have a higher level of variance than in other plant species. Expression of transcripts associated with circadian controlled biological processes is largely conserved between wheat and Arabidopsis; however, striking differences are seen in agriculturally critical processes such as starch metabolism. Together, this work highlights the ongoing selection for balance versus diversification in circadian homoeologs and identifies clock-controlled pathways that might provide important targets for future wheat breeding.
Subject(s)
Arabidopsis , Circadian Clocks , Arabidopsis/genetics , Circadian Clocks/genetics , Circadian Rhythm/genetics , Gene Expression Regulation, Plant/genetics , Plant Breeding , Polyploidy , Starch/metabolism , Transcriptome/genetics , Triticum/geneticsABSTRACT
Circadian rhythms are 24-h biological cycles that align metabolism, physiology, and development with daily environmental fluctuations. Photosynthetic processes are governed by the circadian clock in both flowering plants and some cyanobacteria, but it is unclear how extensively this is conserved throughout the green lineage. We investigated the contribution of circadian regulation to aspects of photosynthesis in Marchantia polymorpha, a liverwort that diverged from flowering plants early in the evolution of land plants. First, we identified in M. polymorpha the circadian regulation of photosynthetic biochemistry, measured using two approaches (delayed fluorescence, pulse amplitude modulation fluorescence). Second, we identified that light-dark cycles synchronize the phase of 24 h cycles of photosynthesis in M. polymorpha, whereas the phases of different thalli desynchronize under free-running conditions. This might also be due to the masking of the underlying circadian rhythms of photosynthesis by light-dark cycles. Finally, we used a pharmacological approach to identify that chloroplast translation might be necessary for clock control of light-harvesting in M. polymorpha. We infer that the circadian regulation of photosynthesis is well-conserved amongst terrestrial plants.
Subject(s)
Circadian Clocks , Embryophyta , Marchantia , Circadian Rhythm , Marchantia/genetics , Marchantia/metabolism , PhotosynthesisABSTRACT
Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade-avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early-evening expression of the central circadian-clock components TIMING OF CAB EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3), and ELF4 in photocycles of low R:FR and low PAR. These collectively suppress stem elongation, antagonizing shade avoidance in deep canopy shade.
Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/physiology , Circadian Clocks , Phytochrome A/metabolism , Plant Leaves/physiology , Arabidopsis/genetics , Arabidopsis/radiation effects , Arabidopsis Proteins/genetics , Circadian Clocks/radiation effects , Circadian Rhythm/radiation effects , Gene Expression Regulation, Plant , Light , Plant Leaves/radiation effects , RNA, Messenger/genetics , RNA, Messenger/metabolismABSTRACT
Circadian regulation has a pervasive influence upon plant development, physiology and metabolism, impacting upon components of fitness and traits of agricultural importance. Circadian regulation is inextricably connected to the responses of plants to their abiotic environments, from the cellular to whole plant scales. Here, we review the crosstalk that occurs between circadian regulation and responses to the abiotic environment from the intracellular scale through to naturally fluctuating environments. We examine the spatial crosstalk that forms part of plant circadian regulation, at the subcellular, tissue, organ and whole-plant scales. This includes a focus on chloroplast and mitochondrial signalling, alternative splicing, long-distance circadian signalling and circadian regulation within natural environments. We also consider mathematical models for plant circadian regulation, to suggest future areas for advancing understanding of roles for circadian regulation in plant responses to environmental cues.
Subject(s)
Circadian Clocks , Circadian Rhythm , Environment , Plants/metabolism , Signal Transduction , Alternative Splicing , Gene Expression Regulation, Plant , Plant Development , Plants/geneticsABSTRACT
Circadian clocks create a 24-hour temporal structure, which allows organisms to occupy a niche formed by time rather than space. They are pervasive throughout nature, yet they remain unexpectedly unexplored and uncharacterized in nonphotosynthetic bacteria. Here, we identify in Bacillus subtilis circadian rhythms sharing the canonical properties of circadian clocks: free-running period, entrainment, and temperature compensation. We show that gene expression in B. subtilis can be synchronized in 24-hour light or temperature cycles and exhibit phase-specific characteristics of entrainment. Upon release to constant dark and temperature conditions, bacterial biofilm populations have temperature-compensated free-running oscillations with a period close to 24 hours. Our work opens the field of circadian clocks in the free-living, nonphotosynthetic prokaryotes, bringing considerable potential for impact upon biomedicine, ecology, and industrial processes.
ABSTRACT
Trichomes are large epidermal cells on the surface of leaves that are thought to deter herbivores, yet the presence of trichomes can also negatively impact plant growth and reproduction. Stomatal guard cells and trichomes have shared developmental origins, and experimental manipulation of trichome formation can lead to changes in stomatal density. The influence of trichome formation upon stomatal development in natural populations of plants is currently unknown. Here, we show that a natural population of Arabidopsis halleri that includes hairy (trichome-bearing) and glabrous (no trichomes) morphs has differences in stomatal density that are associated with this trichome dimorphism. We found that glabrous morphs had significantly greater stomatal density and stomatal index than hairy morphs. One interpretation is that this arises from a trade-off between the proportions of cells that have trichome and guard cell fates during leaf development. The differences in stomatal density between the two morphs might have impacts upon environmental adaptation, in addition to herbivory deterrence caused by trichome development.
ABSTRACT
Vertical farming is a type of indoor agriculture where plants are cultivated in stacked systems. It forms a rapidly growing sector with new emerging technologies. Indoor farms often use soil-free techniques such as hydroponics and aeroponics. Aeroponics involves the application to roots of a nutrient aerosol, which can lead to greater plant productivity than hydroponic cultivation. Aeroponics is thought to resolve a variety of plant physiological constraints that occur within hydroponic systems. We synthesize existing studies of the physiology and development of crops cultivated under aeroponic conditions and identify key knowledge gaps. We identify future research areas to accelerate the sustainable intensification of vertical farming using aeroponic systems.
Subject(s)
Agriculture , Plant Roots , Crops, Agricultural , Farms , HydroponicsABSTRACT
In plants, water use efficiency (WUE) is a complex trait arising from numerous physiological and developmental characteristics. Here, we investigated the involvement of circadian regulation in long-term WUE in Arabidopsis (Arabidopsis thaliana) under light and dark conditions. Circadian rhythms are generated by the circadian oscillator, which provides a cellular measure of the time of day. In plants, the circadian oscillator contributes to the regulation of many aspects of physiology, including stomatal opening, rate of photosynthesis, carbohydrate metabolism, and developmental processes such as the initiation of flowering. We investigated the impact of the misregulation of numerous genes encoding various components of the circadian oscillator on whole plant, long-term WUE. From this analysis, we identified a role for the circadian oscillator in WUE. It appears that the circadian clock contributes to the control of transpiration and biomass accumulation. We also established that the circadian oscillator within guard cells can contribute to long-term WUE. Our experiments indicate that knowledge of circadian regulation will be important for developing crops with improved WUE.
Subject(s)
Arabidopsis/metabolism , Arabidopsis/physiology , Circadian Clocks/physiology , Water/metabolism , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Circadian Clocks/genetics , Circadian Rhythm/genetics , Circadian Rhythm/physiology , Gene Expression Regulation, Plant , Photosynthesis/genetics , Photosynthesis/physiology , Plant Transpiration/genetics , Plant Transpiration/physiologyABSTRACT
High temperature promotes guard cell expansion, which opens stomatal pores to facilitate leaf cooling. How the high-temperature signal is perceived and transmitted to regulate stomatal aperture is, however, unknown. Here, we used a reverse-genetics approach to understand high temperature-mediated stomatal opening in Arabidopsis (Arabidopsis thaliana). Our findings reveal that high temperature-induced guard cell movement requires components involved in blue light-mediated stomatal opening, suggesting cross talk between light and temperature signaling pathways. The molecular players involved include phototropin photoreceptors, plasma membrane H+-ATPases, and multiple members of the 14-3-3 protein family. We further show that phototropin-deficient mutants display impaired rosette evapotranspiration and leaf cooling at high temperatures. Blocking the interaction of 14-3-3 proteins with their client proteins severely impairs high temperature-induced stomatal opening but has no effect on the induction of heat-sensitive guard cell transcripts, supporting the existence of an additional intracellular high-temperature response pathway in plants.