Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis

Chang, Katherine N.; Zhong, Shan; Weirauch, Matthew T.; Hon, Gary C.; Pelizzola, Mattia; Li, Hai; Huang, S.; Schmitz, Robert J.; Urich, Mark A.; Kuo, Dwight; Nery, Joseph R.; Qiao, Hong; Yang, Ally; Jamali, Abdullah; Chen, Huaming; Ideker, Trey; Ren, Bing; Bar‐Joseph, Ziv; Hughes, Timothy R.; Ecker, Joseph R.

doi:10.7554/elife.00675

Cited by 392 publications

(521 citation statements)

References 77 publications

(109 reference statements)

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“…For ABI5, ANAC055, and HB5 ChIP-seq, the YPET or wildtype lines were germinated and grown for 36 hr under dark or long day light conditions. ChIP-seq was carried out as previously described with minor modifications (Chang et al, 2013).…”

Section: Experimental Procedures Dap-seq and Chip-seq Experimentsmentioning

confidence: 99%

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

O’Malley¹,

Huang²,

Song³

et al. 2016

Cell

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SUMMARYThe cistrome is the complete set of transcription factor (TF) binding sites (cis-elements) in an organism, while an epicistrome incorporates tissue-specific DNA chemical modifications and TFspecific chemical sensitivities into these binding profiles. Robust methods to construct comprehensive cistrome and epicistrome maps are critical for elucidating complex transcriptional networks that underlie growth, behavior, and disease. Here, we describe DNA affinity purification sequencing (DAP-seq), a high-throughput TF binding site discovery method that interrogates genomic DNA with in-vitro-expressed TFs. Using DAP-seq, we defined the Arabidopsis cistrome by resolving motifs and peaks for 529 TFs. Because genomic DNA used in DAP-seq retains 5-methylcytosines, we determined that >75% (248/327) of Arabidopsis TFs surveyed were methylation sensitive, a property that strongly impacts the epicistrome landscape. DAP-seq datasets also yielded insight into the biology and binding site architecture of numerous TFs, demonstrating the value of DAP-seq for cost-effective cistromic and epicistromic annotation in any organism.

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Section: Experimental Procedures Dap-seq and Chip-seq Experimentsmentioning

confidence: 99%

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

O’Malley¹,

Huang²,

Song³

et al. 2016

Cell

Self Cite

373

482

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show abstract

“…An overview of which replicates were used for the samples is provided in Supplemental Table 4. For EIN3, the time point at which the maximal number of binding events occurred (4 h) was processed (Chang et al, 2013). REV, AMS, and FLP/MYB88 were removed from the data set due to a very low number of peaks in the results, the lack of paired-end read processing in the computational pipeline, and an abnormally high fraction of peak regions near transposable elements (Supplemental Figure 2A), respectively.…”

Section: Chip-seq Processingmentioning

confidence: 99%

A Functional and Evolutionary Perspective on Transcription Factor Binding in Arabidopsis thaliana

et al. 2014

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Understanding the mechanisms underlying gene regulation is paramount to comprehend the translation from genotype to phenotype. The two are connected by gene expression, and it is generally thought that variation in transcription factor (TF) function is an important determinant of phenotypic evolution. We analyzed publicly available genome-wide chromatin immunoprecipitation experiments for 27 TFs in Arabidopsis thaliana and constructed an experimental network containing 46,619 regulatory interactions and 15,188 target genes. We identified hub targets and highly occupied target (HOT) regions, which are enriched for genes involved in development, stimulus responses, signaling, and gene regulatory processes in the currently profiled network. We provide several lines of evidence that TF binding at plant HOT regions is functional, in contrast to that in animals, and not merely the result of accessible chromatin. HOT regions harbor specific DNA motifs, are enriched for differentially expressed genes, and are often conserved across crucifers and dicots, even though they are not under higher levels of purifying selection than non-HOT regions. Distal bound regions are under purifying selection as well and are enriched for a chromatin state showing regulation by the Polycomb repressive complex. Gene expression complexity is positively correlated with the total number of bound TFs, revealing insights in the regulatory code for genes with different expression breadths. The integration of noncanonical and canonical DNA motif information yields new hypotheses on cobinding and tethering between specific TFs involved in flowering and light regulation.

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“…RAP2.3 represents an EIN3-dependent branch of ethylene signaling, formerly exemplified by ERF1 (Solano et al, 1998), which participates in the transcriptional cascade triggered by the hormone in the control of this developmental process. RAP2.3 regulates sets of genes that are not directly regulated by EIN3, which is the case of three of four genes shown in Figure 4 (Chang et al, 2013), expanding this way the effect on gene expression triggered by ethylene. Interestingly, HLS1, a major target of EIN3 in the regulation of hook development, is not an in vivo target of RAP2.3, because (1) its expression was not altered after RAP2.3 induction or in the rap2.3 mutant (Supplemental Fig.…”

Section: Resultsmentioning

confidence: 99%

“…It was previously shown that RAP2.3 expression is induced by ethylene (Büttner and Singh, 1997). Significantly, EIN3 binds in vivo to the RAP2.3 promoter (Chang et al, 2013) and activates its expression in etiolated seedlings (Fig. 6A), suggesting that RAP2.3 could also participate in the mechanism regulating apical hook development by GAs and ethylene.…”

Section: Dellas Prevent the Binding Of Rap23 To The Promoter Of Itsmentioning

confidence: 99%

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Large-Scale Identification of Gibberellin-Related Transcription Factors Defines Group VII ETHYLENE RESPONSE FACTORS as Functional DELLA Partners

et al. 2014

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DELLA proteins are the master negative regulators in gibberellin (GA) signaling acting in the nucleus as transcriptional regulators. The current view of DELLA action indicates that their activity relies on the physical interaction with transcription factors (TFs). Therefore, the identification of TFs through which DELLAs regulate GA responses is key to understanding these responses from a mechanistic point of view. Here, we have determined the TF interactome of the Arabidopsis (Arabidopsis thaliana) DELLA protein GIBBERELLIN INSENSITIVE and screened a collection of conditional TF overexpressors in search of those that alter GA sensitivity. As a result, we have found RELATED TO APETALA2.3, an ethylene-induced TF belonging to the group VII ETHYLENE RESPONSE FACTOR of the APETALA2/ethylene responsive element binding protein superfamily, as a DELLA interactor with physiological relevance in the context of apical hook development. The combination of transactivation assays and chromatin immunoprecipitation indicates that the interaction with GIBBERELLIN INSENSITIVE impairs the activity of RELATED TO APETALA2.3 on the target promoters. This mechanism represents a unique node in the cross regulation between the GA and ethylene signaling pathways controlling differential growth during apical hook development.

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Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis

Cited by 392 publications

References 77 publications

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

A Functional and Evolutionary Perspective on Transcription Factor Binding in Arabidopsis thaliana

Large-Scale Identification of Gibberellin-Related Transcription Factors Defines Group VII ETHYLENE RESPONSE FACTORS as Functional DELLA Partners

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