An official website of the United States government
Abstract The circadian clock is an internal molecular oscillator and coordinates numerous physiological processes through regulation of molecular pathways. Tissue‐specific clocks connected by mobile signals have previously been found to run at different speeds inArabidopsis thalianatissues. However, tissue variation in circadian clocks in crop species is unknown. In this study, leaf and tuber global gene expression in cultivated potato under cycling and constant environmental conditions was profiled. In addition, we used a circadian‐regulated luciferase reporter construct to study tuber gene expression rhythms. Diel and circadian expression patterns were present among 17.9% and 5.6% of the expressed genes in the tuber. Over 500 genes displayed differential tissue specific diel phases. Intriguingly, few core circadian clock genes had circadian expression patterns, while all such genes were circadian rhythmic in cultivated tomato leaves. Furthermore, robust diel and circadian transcriptional rhythms were observed among detached tubers. Our results suggest alternative regulatory mechanisms and/or clock composition is present in potato, as well as the presence of tissue‐specific independent circadian clocks. We have provided the first evidence of a functional circadian clock in below‐ground storage organs, holding important implications for other storage root and tuberous crops.
more »
« less
Temperature-driven coordination of circadian transcriptional regulation
The circadian clock is an evolutionarily-conserved molecular oscillator that enables species to anticipate rhythmic changes in their environment. At a molecular level, the core clock genes induce circadian oscillations in thousands of genes in a tissue–specific manner, orchestrating myriad biological processes. While previous studies have investigated how the core clock circuit responds to environmental perturbations such as temperature, the downstream effects of such perturbations on circadian regulation remain poorly understood. By analyzing bulk-RNA sequencing ofDrosophilafat bodies harvested from flies subjected to different environmental conditions, we demonstrate a highly condition-specific circadian transcriptome: genes are cycling in a temperature-specific manner, and the distributions of their phases also differ between the two conditions. Further employing a reference-based gene regulatory network (Reactome), we find evidence of increased gene-gene coordination at low temperatures and synchronization of rhythmic genes that are network neighbors. We report that the phase differences between cycling genes increase as a function of geodesic distance in the low temperature condition, suggesting increased coordination of cycling on the gene regulatory network. Our results suggest a potential mechanism whereby the circadian clock mediates the fly’s response to seasonal changes in temperature.
more »
« less
- Award ID(s):
- 1764421
- PAR ID:
- 10525838
- Editor(s):
- Bollenbach, Tobias
- Publisher / Repository:
- PLoS
- Date Published:
- Journal Name:
- PLOS Computational Biology
- Volume:
- 20
- Issue:
- 4
- ISSN:
- 1553-7358
- Page Range / eLocation ID:
- e1012029
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Organisms track time of day through the function of cell-autonomous molecular clocks. In addition to a central clock located in the brain, molecular clocks are present in most peripheral tissues. Circadian clocks are coordinated within and across tissues, but the manner through which this coordination is achieved is not well understood. We reasoned that the ability to track in vivo molecular clock activity in specific tissues of the fruit fly, Drosophila melanogaster, would facilitate an investigation into the relationship between different clock-containing tissues. Previous efforts to monitor clock gene expression in single flies in vivo have used regulatory elements of several different clock genes to dictate expression of a luciferase reporter enzyme, the activity of which can be monitored using a luminometer. Although these reporter lines have been instrumental in our understanding of the circadian system, they generally lack cell specificity, making it difficult to compare molecular clock oscillations between different tissues. Here, we report the generation of several novel lines of flies that allow for inducible expression of a luciferase reporter construct for clock gene transcriptional activity. We find that these lines faithfully report circadian transcription, as they exhibit rhythmic luciferase activity that is dependent on a functional molecular clock. Furthermore, we take advantage of our reporter lines’ tissue specificity to demonstrate that peripheral molecular clocks are able to retain rhythmicity for multiple days under constant environmental conditions.more » « less
-
Penfield, Steve (Ed.)Abstract The transcriptomes of many eukaryotic genomes exhibit rhythmic gene expression, resulting in genes that show peak expression at specific times of the day. In plants, genes that are considered to be oscillator components alter the circadian period and/or phase (time of peak expression) when misexpressed. The first plant circadian clock gene was identified almost 30 years ago, and since then additional components have been identified through forward and reverse genetic mutant screens. Over the years, mathematical modeling has helped to refine our understanding of oscillator interactions within the network and in the context of environmental cues. The complexity of the clock network suggests that additional components are yet to be discovered. In the era of genomics and genome-scale analysis, circadian research has focused on understanding the mechanisms of clock gene control of cellular and physiological output processes, often in the context of environmental stimuli. Transcriptome studies with temporal and/or spatial resolution are increasingly being carried out and the resulting comprehensive datasets can be mined to predict new oscillator components. Most clock genes show stronger oscillatory expression patterns compared to other genes in the genome. By selecting from transcriptome data genes that are significantly and robustly rhythmic, putative clock genes can be identified and characterized.more » « less
-
SUMMARY Sorghum is one of the four major C4 crops that are considered to be tolerant to environmental extremes. Sorghum shows distinct growth responses to temperature stress depending on the sensitivity of the genetic background. About half of the transcripts in sorghum exhibit diurnal rhythmic expressions emphasizing significant coordination with the environment. However, an understanding of how molecular dynamics contribute to genotype‐specific stress responses in the context of the time of day is not known. We examined whether temperature stress and the time of day impact the gene expression dynamics in thermo‐sensitive and thermo‐tolerant sorghum genotypes. We found that time of day is highly influencing the temperature stress responses, which can be explained by the rhythmic expression of most thermo‐responsive genes. This effect is more pronounced in thermo‐tolerant genotypes, suggesting a stronger regulation of gene expression by the time of day and/or by the circadian clock. Genotypic differences were mostly observed on average gene expression levels, which may be responsible for contrasting sensitivities to temperature stress in tolerant versus susceptible sorghum varieties. We also identified groups of genes altered by temperature stress in a time‐of‐day and genotype‐specific manner. These include transcriptional regulators and several members of the Ca2+‐binding EF‐hand protein family. We hypothesize that expression variation of these genes between genotypes along with time‐of‐day independent regulation may contribute to genotype‐specific fine‐tuning of thermo‐responsive pathways. These findings offer a new opportunity to selectively target specific genes in efforts to develop climate‐resilient crops based on their time‐of‐day and genotype variation responses to temperature stress.more » « less
-
Fay, Justin C. (Ed.)Circadian rhythms are nearly ubiquitous throughout nature, suggesting they are critical for survival in diverse environments. Organisms inhabiting largely arrhythmic environments, such as caves, offer a unique opportunity to study the evolution of circadian rhythms in response to changing ecological pressures. Populations of the Mexican tetra, Astyanax mexicanus , have repeatedly invaded caves from surface rivers, where individuals must contend with perpetual darkness, reduced food availability, and limited fluctuations in daily environmental cues. To investigate the molecular basis for evolved changes in circadian rhythms, we investigated rhythmic transcription across multiple independently-evolved cavefish populations. Our findings reveal that evolution in a cave environment has led to the repeated disruption of the endogenous biological clock, and its entrainment by light. The circadian transcriptome shows widespread reductions and losses of rhythmic transcription and changes to the timing of the activation/repression of core-transcriptional clock. In addition to dysregulation of the core clock, we find that rhythmic transcription of the melatonin regulator aanat2 and melatonin rhythms are disrupted in cavefish under darkness. Mutants of aanat2 and core clock gene rorca disrupt diurnal regulation of sleep in A . mexicanus , phenocopying circadian modulation of sleep and activity phenotypes of cave populations. Together, these findings reveal multiple independent mechanisms for loss of circadian rhythms in cavefish populations and provide a platform for studying how evolved changes in the biological clock can contribute to variation in sleep and circadian behavior.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pcbi.1012029
