Crosstalk between the Circadian Clock and Innate Immunity in Arabidopsis

Zhang, Chong; Xie, Qiguang; Anderson, Ryan; Ng, Gina; Seitz, Nicholas; Peterson, Thomas; McClung, C. Robertson; McDowell, John M.; Kong, Dongdong; Kwak, June M.; Lu, Hua

doi:10.1371/journal.ppat.1003370

Cited by 168 publications

(215 citation statements)

References 91 publications

(169 reference statements)

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“…Consistent with the known role of CCA1 in regulating responses to abiotic and biotic stresses, we observe enrichment in genes with GO terms associated with response to both biotic and abiotic stresses, including response to low temperature and light ( Fig. S1E) (8,9,25,(33)(34)(35). Putative CCA1 targets also are enriched for genes involved in hormone response, including gibberellic acid and abscisic acid, as is consistent with the known role of the circadian clock in the regulation of daily cycles of hormone sensitivity (22,36).…”

Section: Countsupporting

confidence: 84%

Genome-wide identification of CCA1 targets uncovers an expanded clock network inArabidopsis

Nagel

Doherty

Pruneda‐Paz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

234

279

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The circadian clock in Arabidopsis exerts a critical role in timing multiple biological processes and stress responses through the regulation of up to 80% of the transcriptome. As a key component of the clock, the Myb-like transcription factor CIRCADIAN CLOCK ASSOCIATED1 (CCA1) is able to initiate and set the phase of clockcontrolled rhythms and has been shown to regulate gene expression by binding directly to the evening element (EE) motif found in target gene promoters. However, the precise molecular mechanisms underlying clock regulation of the rhythmic transcriptome, specifically how clock components connect to clock output pathways, is poorly understood. In this study, using ChIP followed by deep sequencing of CCA1 in constant light (LL) and diel (LD) conditions, more than 1,000 genomic regions occupied by CCA1 were identified. CCA1 targets are enriched for a myriad of biological processes and stress responses, providing direct links to clock-controlled pathways and suggesting that CCA1 plays an important role in regulating a large subset of the rhythmic transcriptome. Although many of these target genes are evening expressed and contain the EE motif, a significant subset is morning phased and enriched for previously unrecognized motifs associated with CCA1 function. Furthermore, this work revealed several CCA1 targets that do not cycle in either LL or LD conditions. Together, our results emphasize an expanded role for the clock in regulating a diverse category of genes and key pathways in Arabidopsis and provide a comprehensive resource for future functional studies.genome-wide | circadian clock | clock-controlled outputs | transcriptional regulation I n anticipation of the daily changes in light and temperature, the plant's internal circadian clock regulates a large portion of the transcriptome, nearly 80% in rice, poplar, and Arabidopsis (1, 2). The clock provides temporal coordination of multiple biological functions to ensure optimal efficiency. For example, before dawn, photosynthetic transcripts accumulate in anticipation of the expected sunlight. Even when shifted to constant light (LL) and temperature, in the absence of day/night cues, transcripts associated with photosynthesis are still up-regulated before the subjective day (1-4). Not only are light-and energyrelated activities restricted to particular times, but other aspects of plant growth, including water use, hormone activity, UVB response, and low-temperature response, show this gating effect (5-9). This temporal partitioning of biological responses ultimately provides an optimal integration of the plant's organismal functions with the environment.The circadian clock in plants involves a posttranscriptional component and a well-studied transcriptional-translation feedback regulation between the Myb-like transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) and a member of the PSEUDO RESPONSE REGULATOR (PRR) family, TIMING OF CAB2 EXPRESSION 1 (TOC1) (10-16). Together these three components contribute t...

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Section: Countsupporting

confidence: 84%

Genome-wide identification of CCA1 targets uncovers an expanded clock network inArabidopsis

Nagel

Doherty

Pruneda‐Paz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

234

279

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“…The Arabidopsis thaliana Columbia-0 ecotype (Col-0) or Wassilewskija (Ws) was used unless otherwise indicated. The CCA1:LUC + (Col-0), CCA1::GFP-CCA1, CCA1-OX (Col-0), and cca1-1/lhy-21 (Ws and Col-0) lines were described previously (33,36,43). The FBH1 amiRNA lines amiRFBH1-1 (2-7) and amiRFBH1-2 (3-5) were reported previously (27).…”

Section: Methodsmentioning

confidence: 99%

FBH1 affects warm temperature responses in the Arabidopsis circadian clock

Nagel

Pruneda‐Paz

Kay

2014

Proc. Natl. Acad. Sci. U.S.A.

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In Arabidopsis, the circadian clock allows the plant to coordinate daily external signals with internal processes, conferring enhanced fitness and growth vigor. Although external cues such as temperature can entrain the clock, an important feature of the clock is the ability to maintain a relatively constant period over a range of physiological temperatures; this ability is referred to as "temperature compensation." However, how temperature actually is perceived and integrated into the clock molecular circuitry remains largely unknown. In an effort to identify additional regulators of the circadian clock, including putative components that could modulate the clock response to changes in environmental signals, we identified in a previous large-scale screen a transcription factor that interacts with and regulates the promoter activity of a core clock gene. In this report, we characterized this transcription factor, FLOWERING BASIC HELIX-LOOP-HELIX 1 (FBH1) that binds in vivo to the promoter of the key clock gene CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and regulates its expression. We found that upon temperature changes, overexpression of FBH1 alters the pace of CCA1 expression by causing a period shortening and thus preventing the clock from buffering against this change in temperature. Furthermore, as is consistent with the current mechanistic model of feedback loops observed in the clock regulatory network, we also determined that CCA1 binds in vivo to the FBH1 promoter and regulates its expression. Together these results establish a role for FBH1 as a transcriptional modulator of warm temperature signals and clock responses in Arabidopsis.T o adapt better to the daily and seasonal environmental changes, most organisms have an internal timekeeping mechanism known as the "circadian clock." The clock is a self-sustaining machinery that enables organisms to anticipate external fluctuations and in turn coordinate important physiological and developmental processes to occur at optimal times during the day, enhancing fitness (1, 2). In Arabidopsis, the clock consists of a complex network of interlocked regulatory feedback loops between multiple components (3-6). Synchronization of these components with external cues reinforces robust rhythms and allows the clock to coordinate efficiently the regulation of numerous biological outputs such as photosynthesis, photoperiodic flowering, hormone levels, and responses to biotic and abiotic stresses (1,3,(7)(8)(9). Key players in this interconnected network are the transcriptional components CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), two Myb-domain transcription factors, and TIMING OF CAB EXPRESSION 1 (TOC1). These three components, CCA1, LHY, and TOC1, form the core regulatory framework of the Arabidopsis circadian clock; their activity consists of transcriptional repression of each other and direct temporal regulation of most other clock components throughout the day (9-11).Integration and synchronization of environmental signals such as light and te...

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“…In Arabidopsis thaliana, the RNA-directed DNA methylation pathway mediates a parent-of-origin effect on circadian rhythms, leading to biomass heterosis in reciprocal F1 hybrids 18 . In A. thaliana diploids, the circadian clock regulates abiotic 19,20 and biotic [21][22][23] stress responses. However, there is a tradeoff between stress responses and fitness; constitutive expression of stressresponsive genes reduces fitness and growth 24,25 , while repressing disease resistance genes promotes growth 26 .…”

mentioning

confidence: 99%

Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

et al. 2015

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The genetic distance between hybridizing parents affects heterosis; however, the mechanisms for this remain unclear. Here we report that this genetic distance correlates with natural variation and epigenetic regulation of circadian clock-mediated stress responses. In intraspecific hybrids of Arabidopsis thaliana, genome-wide expression of many biotic and abiotic stress-responsive genes is diurnally repressed and this correlates with biomass heterosis and biomass quantitative trait loci. Expression differences of selected stress-responsive genes among diverse ecotypes are predictive of heterosis in their hybrids. Stress-responsive genes are repressed in the hybrids under normal conditions but are induced to mid-parent or higher levels under stress at certain times of the day, potentially balancing the tradeoff between stress responses and growth. Consistent with this hypothesis, repression of two candidate stress-responsive genes increases growth vigour. Our findings may therefore provide new criteria for effectively selecting parents to produce high-or lowyield hybrids.

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Crosstalk between the Circadian Clock and Innate Immunity in Arabidopsis

Cited by 168 publications

References 91 publications

Genome-wide identification of CCA1 targets uncovers an expanded clock network inArabidopsis

Genome-wide identification of CCA1 targets uncovers an expanded clock network inArabidopsis

FBH1 affects warm temperature responses in the Arabidopsis circadian clock

Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

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