Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Changes in ambient temperature are the prevailing cue in determining Brachypodium distachyon diurnal gene regulation

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.16507· OSTI ID:1650702
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [5];  [6];  [3]
  1. Biology Department University of Massachusetts Amherst MA 01003 USA, Molecular and Cellular Biology Graduate Program University of Massachusetts Amherst MA 01003 USA
  2. DOE Joint Genome Institute Walnut Creek CA 94598 USA, Department of Neurology Keck School of Medicine University of Southern California Los Angeles CA 90033 USA
  3. Biology Department University of Massachusetts Amherst MA 01003 USA
  4. Biology Department University of Massachusetts Amherst MA 01003 USA, Plant Biology Graduate Program University of Massachusetts Amherst MA 01003 USA
  5. J. Craig Venter Institute La Jolla CA 92037 USA
  6. Department of Neurology Keck School of Medicine University of Southern California Los Angeles CA 90033 USA
Summary

Plants are continuously exposed to diurnal fluctuations in light and temperature, and spontaneous changes in their physical or biotic environment. The circadian clock coordinates regulation of gene expression with a 24 h period, enabling the anticipation of these events.

We used RNA sequencing to characterize the Brachypodium distachyon transcriptome under light and temperature cycles, as well as under constant conditions.

Approximately 3% of the transcriptome was regulated by the circadian clock, a smaller proportion than reported in most other species. For most transcripts that were rhythmic under all conditions, including many known clock genes, the period of gene expression lengthened from 24 to 27 h in the absence of external cues. To functionally characterize the cyclic transcriptome in B. distachyon , we used Gene Ontology enrichment analysis, and found several terms significantly associated with peak expression at particular times of the day. Furthermore, we identified sequence motifs enriched in the promoters of similarly phased genes, some potentially associated with transcription factors.

When considering the overlap in rhythmic gene expression and specific pathway behavior, thermocycles was the prevailing cue that controlled diurnal gene regulation. Taken together, our characterization of the rhythmic B. distachyon transcriptome represents a foundational resource with implications in other grass species.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0006621
OSTI ID:
1650702
Alternate ID(s):
OSTI ID: 1801700
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 6 Vol. 227; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (113)

Cross-species complementation reveals conserved functions for EARLY FLOWERING 3 between monocots and dicots journal October 2017
Wilcoxon Rank Sum Test book January 2013
ggplot2 book January 2016
Evolutionary Relationships Among Barley and Arabidopsis Core Circadian Clock and Clock-Associated Genes journal January 2015
Conserved Daily Transcriptional Programs in Carica papaya journal December 2008
Basic local alignment search tool journal October 1990
H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis journal January 2010
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape journal May 2016
Overlapping and Distinct Roles of PRR7 and PRR9 in the Arabidopsis Circadian Clock journal January 2005
Complexity in the Wiring and Regulation of Plant Circadian Networks journal January 2013
Transcriptional Regulation of LUX by CBF1 Mediates Cold Input to the Circadian Clock in Arabidopsis journal July 2014
ELF3-PIF4 Interaction Regulates Plant Growth Independently of the Evening Complex journal January 2015
ELF3 Controls Thermoresponsive Growth in Arabidopsis journal January 2015
A Localized Pseudomonas syringae Infection Triggers Systemic Clock Responses in Arabidopsis journal February 2018
Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63 journal August 2018
Multi-level Modulation of Light Signaling by GIGANTEA Regulates Both the Output and Pace of the Circadian Clock journal June 2019
Role of circadian rhythm in plant system: An update from development to stress response journal June 2019
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities journal May 2010
Circadian Clock Genes Universally Control Key Agricultural Traits journal August 2015
WRKY transcription factors: from DNA binding towards biological function journal October 2004
Role of Temperature in the Regulation of Leaf Extension in Zea mays journal January 1971
The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops journal January 2012
Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana journal December 2003
Rhythmic growth explained by coincidence between internal and external cues journal June 2007
The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth journal July 2011
Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis journal April 2011
HISAT: a fast spliced aligner with low memory requirements journal March 2015
Molecular mechanisms at the core of the plant circadian oscillator journal December 2016
Kingdom-wide comparison reveals the evolution of diurnal gene expression in Archaeplastida journal February 2019
Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis journal January 1999
Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock journal January 2010
Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor journal February 2012
Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana journal August 2012
LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator journal July 2013
Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis journal August 2015
Circadian control of ORE1 by PRR9 positively regulates leaf senescence in Arabidopsis journal July 2018
Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit journal February 1997
Quantitative Circadian Phosphoproteomic Analysis of Arabidopsis Reveals Extensive Clock Control of Key Components in Physiological, Metabolic, and Signaling Pathways journal June 2015
Analyzing circadian expression data by harmonic regression based on autoregressive spectral estimation journal June 2010
MetaCycle: an integrated R package to evaluate periodicity in large scale data journal July 2016
Light, the circadian clock, and sugar perception in the control of lignin biosynthesis journal May 2005
Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects journal March 2010
Interaction of light and temperature signalling journal February 2014
How Do Phytochromes Transmit the Light Quality Information to the Circadian Clock in Arabidopsis ? journal November 2014
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform journal July 2002
Phytozome: a comparative platform for green plant genomics journal November 2011
limma powers differential expression analyses for RNA-sequencing and microarray studies journal January 2015
g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update) journal May 2019
Comparative Overviews of Clock-Associated Genes of Arabidopsis thaliana and Oryza sativa journal January 2007
Ambient Temperature Signal Feeds into the Circadian Clock Transcriptional Circuitry Through the EC Night-Time Repressor in Arabidopsis thaliana journal March 2014
Diurnal.plant.tools: Comparative Transcriptomic and Co-expression Analyses of Diurnal Gene Expression of the Archaeplastida Kingdom journal September 2019
Root Transformation of Arabidopsis journal December 2006
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis journal January 2007
Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants journal May 2002
Quantitative Statistical Analysis of cis-Regulatory Sequences in ABA/VP1- and CBF/DREB1-Regulated Genes of Arabidopsis journal August 2005
Disruption of the Arabidopsis Circadian Clock Is Responsible for Extensive Variation in the Cold-Responsive Transcriptome journal March 2008
Independent Action of ELF3 and phyB to Control Hypocotyl Elongation and Flowering Time journal April 2000
A G-Box-Like Motif Is Necessary for Transcriptional Regulation by Circadian Pseudo-Response Regulators in Arabidopsis journal November 2015
Decoys Untangle Complicated Redundancy and Reveal Targets of Circadian Clock F-Box Proteins journal May 2018
Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis journal August 1998
FLOWERING LOCUS C Mediates Natural Variation in the High-Temperature Response of the Arabidopsis Circadian Clock journal February 2006
A Reduced-Function Allele Reveals That EARLY FLOWERING3 Repressive Action on the Circadian Clock Is Modulated by Phytochrome Signals in Arabidopsis journal September 2011
Alternative Splicing Mediates Responses of the Arabidopsis Circadian Clock to Temperature Changes journal March 2012
A Self-Regulatory Circuit of CIRCADIAN CLOCK-ASSOCIATED1 Underlies the Circadian Clock Regulation of Temperature Responses in Arabidopsis journal June 2012
LNK1 and LNK2 Are Transcriptional Coactivators in the Arabidopsis Circadian Oscillator journal July 2014
Direct Repression of Evening Genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock journal March 2016
The Arabidopsis sickle Mutant Exhibits Altered Circadian Clock Responses to Cool Temperatures and Temperature-Dependent Alternative Splicing journal September 2016
ZEITLUPE Contributes to a Thermoresponsive Protein Quality Control System in Arabidopsis journal October 2017
TGA1 and G-box binding factors: two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. journal October 1992
Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation: Role of RVE8/LCL5 in the circadian clock journal February 2011
The regulation of plant growth by the circadian clock: Circadian regulation of plant growth journal January 2012
Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon journal June 2017
Light and temperature cues: multitasking receptors and transcriptional integrators journal November 2017
Circadian control of abscisic acid biosynthesis and signalling pathways revealed by genome-wide analysis of LHY binding targets journal September 2018
Shining a light on the Arabidopsis circadian clock journal September 2017
CYCLING DOF FACTOR 1 represses transcription through the TOPLESS co-repressor to control photoperiodic flowering in Arabidopsis journal September 2017
SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae journal September 2018
Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock journal November 2003
Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage journal July 2005
Mapping the Core of the Arabidopsis Circadian Clock Defines the Network Structure of the Oscillator journal March 2012
Phytochromes and Cryptochromes in the Entrainment of the Arabidopsis Circadian Clock journal November 1998
Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock journal December 2000
Phytochrome B integrates light and temperature signals in Arabidopsis journal October 2016
Phytochromes function as thermosensors in Arabidopsis journal October 2016
Environmental Effects on Spatial and Temporal Patterns of Leaf and Root Growth journal June 2009
JTK_CYCLE: An Efficient Nonparametric Algorithm for Detecting Rhythmic Components in Genome-Scale Data Sets journal September 2010
Discovering Biology in Periodic Data through Phase Set Enrichment Analysis (PSEA) journal March 2016
Geographic Variation of Plant Circadian Clock Function in Natural and Agricultural Settings journal December 2016
Guidelines for Genome-Scale Analysis of Biological Rhythms journal October 2017
Coordination of the maize transcriptome by a conserved circadian clock journal January 2010
Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs journal January 2012
Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR journal January 2008
A modern circadian clock in the common angiosperm ancestor of monocots and eudicots journal May 2010
Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development journal January 2008
Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays journal January 2009
Transcription through the eye of a needle: daily and annual cyclic gene expression variation in Douglas-fir needles journal July 2017
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Stable and Efficient Multiple Smoothing Parameter Estimation for Generalized Additive Models journal September 2004
A Morning-Specific Phytohormone Gene Expression Program underlying Rhythmic Plant Growth journal September 2008
Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules journal January 2008
The Functional Interplay between Protein Kinase CK2 and CCA1 Transcriptional Activity Is Essential for Clock Temperature Compensation in Arabidopsis journal November 2010
REVEILLE8 and PSEUDO-REPONSE REGULATOR5 Form a Negative Feedback Loop within the Arabidopsis Circadian Clock journal March 2011
Temporal Shift of Circadian-Mediated Gene Expression and Carbon Fixation Contributes to Biomass Heterosis in Maize Hybrids journal July 2016
Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album journal June 2019
An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets journal August 2007
Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses journal April 2010
Global Profiling of Rice and Poplar Transcriptomes Highlights Key Conserved Circadian-Controlled Pathways and cis-Regulatory Modules journal June 2011
Circadian Rhythms of Sense and Antisense Transcription in Sugarcane, a Highly Polyploid Crop journal August 2013
Daily Changes in Temperature, Not the Circadian Clock, Regulate Growth Rate in Brachypodium distachyon journal June 2014
Circadian Oscillation of the Lettuce Transcriptome under Constant Light and Light–Dark Conditions journal July 2016
Secondary Wall Regulating NACs Differentially Bind at the Promoter at a CELLULOSE SYNTHASE A4 Cis-eQTL journal December 2018
Circadian and Light Regulated Expression of CBFs and their Upstream Signalling Genes in Barley journal August 2017
Accurate timekeeping is controlled by a cycling activator in Arabidopsis journal April 2013

Similar Records

Daily Changes in Temperature, Not the Circadian Clock, Regulate Growth Rate in Brachypodium distachyon
Journal Article · Thu Jun 12 20:00:00 EDT 2014 · PLoS ONE · OSTI ID:1904512

EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon
Journal Article · Wed Jan 05 19:00:00 EST 2022 · Frontiers in Plant Science · OSTI ID:1838543

Related Subjects