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W4230615659 abstract "Full text Figures and data Side by side Abstract eLife digest Introduction Results Discussion Materials and methods Data availability References Decision letter Author response Article and author information Metrics Abstract The gaseous plant hormone ethylene regulates a multitude of growth and developmental processes. How the numerous growth control pathways are coordinated by the ethylene transcriptional response remains elusive. We characterized the dynamic ethylene transcriptional response by identifying targets of the master regulator of the ethylene signaling pathway, ETHYLENE INSENSITIVE3 (EIN3), using chromatin immunoprecipitation sequencing and transcript sequencing during a timecourse of ethylene treatment. Ethylene-induced transcription occurs in temporal waves regulated by EIN3, suggesting distinct layers of transcriptional control. EIN3 binding was found to modulate a multitude of downstream transcriptional cascades, including a major feedback regulatory circuitry of the ethylene signaling pathway, as well as integrating numerous connections between most of the hormone mediated growth response pathways. These findings provide direct evidence linking each of the major plant growth and development networks in novel ways. https://doi.org/10.7554/eLife.00675.001 eLife digest All multicellular organisms, including plants, produce hormones—chemical messengers that are released in one part of an organism but act in another. The binding of hormones to receptor proteins on the surface of target cells activates signal transduction cascades, leading ultimately to changes in the transcription and translation of genes. Ethylene is a gaseous plant hormone that acts at trace levels to stimulate or regulate a variety of processes, including the regulation of plant growth, the ripening of fruit and the shedding of leaves. Plants also produce ethylene in response to wounding, pathogen attack or exposure to environmental stresses, such as extreme temperatures or drought. Although the effects of ethylene on plants are well documented, much less is known about how its functions are controlled and coordinated at the molecular level. Here, Chang et al. reveal how ethylene alters the transcription of DNA into messenger DNA (mRNA) in the plant model organism, Arabidopsis thaliana. Ethylene is known to exert some of its effects via a protein called EIN3, which is a transcription factor that acts as the master regulator of the ethylene signaling pathway. To identify the targets of EIN3, Chang et al. exposed plants to ethylene and then used a technique called ChIP-Seq to identify those regions of the DNA that EIN3 binds to. At the same time, they used genome-wide mRNA sequencing to determine which genes showed altered transcription. Over the course of 24 hr, ethylene induced four distinct waves of transcription, suggesting that discrete layers of transcriptional control are present. EIN3 binding also controlled a multitude of downstream transcriptional cascades, including a major negative feedback loop. Surprisingly, many of the genes that showed altered expression in response to EIN3 binding were also influenced by hormones other than ethylene. In addition to extending our knowledge of the role of EIN3 in coordinating the effects of ethylene, the work of Chang et al. reveals the extensive connectivity between pathways regulated by distinct hormones in plants. The results may also make it easier to identify key players involved in hormone signaling pathways in other plant species. https://doi.org/10.7554/eLife.00675.002 Introduction Despite the importance of the plant hormone ethylene, we lack a comprehensive understanding of how its linear signaling pathway mediates many different morphological responses. The dynamic ethylene physiological response, a rapid growth inhibition independent of the master transcriptional regulator ETHYLENE INSENSITIVE3 (EIN3), followed by an EIN3-dependent sustained growth inhibition, calls for a temporal study of ethylene transcriptional regulation (Binder et al., 2004a). EIN3 has been shown to be necessary and sufficient for the ethylene response and accumulates upon a duration of exogenous ethylene gas treatment (Guo and Ecker, 2003). Although hundreds of ethylene response genes have been identified, because some of the targets of EIN3 are transcription factors (e.g. ETHYLENE RESPONSE FACTOR1 [ERF1]), it is challenging to distinguish immediate early targets from those further downstream. To understand the dynamics of the EIN3-mediated ethylene transcriptional response, we performed a genome-wide study of the ethylene-induced EIN3 protein-DNA interactions using chromatin immunoprecipitation followed by sequencing (ChIP-Seq) and simultaneously determined the repertoire of target genes that are transcriptionally regulated by ethylene (mRNA-Seq). Tracing the transcriptional cascade, we asked if EIN3-mediated genes contribute to a component of the ethylene transcriptional response. For a select number of EIN3 targets that are putative transcriptional regulators, DNA-binding motifs were identified using protein binding microarrays (PBM) and the enrichment for these motifs in the promoters of ethylene response genes was determined. Results We performed ChIP-Seq using a native antibody that recognizes EIN3 (Guo and Ecker, 2003) as well as mRNA-Seq in three-day-old dark grown seedlings during a timecourse of ethylene treatment (Figure 1—figure supplements 1, 2; Supplementary file 1A). By stringent analysis of the temporal ChIP-Seq data (see ‘Materials and methods’), we identified 1460 EIN3 binding regions in the Arabidopsis genome associated with 1314 genes (Supplementary file 1B). We refer to genes associated with EIN3 binding regions as EIN3 candidate targets. In the sequences of EIN3 binding regions, we found significant enrichment of the consensus TEIL motif (Hypergeometric p<10−87) (Kosugi and Ohashi, 2000), and de novo motif analysis identified the known EIN3 motif (Figure 1—figure supplement 3). We detected three previously described EIN3 targets using our stringent analysis (Figure 1—figure supplements 3, 4) (Solano et al., 1998; Konishi and Yanagisawa, 2008; Chen et al., 2009; Zhong et al., 2009; Boutrot et al., 2010). One example of a known target of EIN3, EIN3-BINDING F-BOX PROTEIN 2 (EBF2), is shown in Figure 1A. EBF2 directs the proteolysis of EIN3 and exhibits ethylene-induced transcription (Figure 1A), resulting in feedback regulation of the ethylene signaling pathway. Our study identified additional distal EIN3 binding in the EBF2 promoter region (Figure 1A, Figure 1—figure supplement 4). Figure 1 with 5 supplements see all Download asset Open asset Dynamics of ethylene-induced EIN3 binding and transcription supports the role of EIN3 as an activator of the ethylene response. (A) Ethylene treatment results in an increase of EIN3 binding in three regions of the EBF2 promoter, corresponding to an increase in steady-state mRNA levels. Binding and transcription levels are indicated by reads per kilobase per million reads in sample (RPKM). Gene model: green (exon), red (UTR), grey (intron/transposon). (B) Patterns of EIN3 binding and expression of ethylene-regulated targets are strikingly evident over a timecourse of ethylene gas treatment. EIN3 binding increases with ethylene treatment to a maximum at 4 hr of ethylene treatment for all candidate targets. Each line in the heatmap represents the RPKM value for the representative EIN3 binding site (left panel) and transcript (right panel). (C) (Upper panel) Equivalent numbers of genes are up- and down-regulated upon ethylene treatment. (Lower panel) Majority of EIN3 targets differentially expressed upon ethylene treatment are up-regulated. (D) A subset of EIN3 targets is transcriptionally regulated by ethylene (EIN3-R). https://doi.org/10.7554/eLife.00675.003 The majority of studies that exist in the literature have shown that EIN3 acts as an activator, and we observed this activation at the genome-wide level (Figure 1B). We found that a majority of EIN3 candidate targets that are regulated by ethylene (referred to as EIN3-R) are induced (85%), Moreover, when compared to the regulation of all genes that respond to ethylene, we observed an over-representation of up-regulation of EIN3 candidate targets (Figure 1B,C). Interestingly, many EIN3-R are transcription factors (∼14%); EIN3 candidate targets are significantly enriched in gene ontology (GO) terms related to transcription factor regulation, confirming that EIN3 activates a transcriptional cascade (Figure 1—figure supplement 5; Supplementary file 1C) (Maere, 2005). Numerous studies have reported that transcription factor binding does not necessarily coincide with changes in transcription (Macquarrie et al., 2011; Menet et al., 2012), especially for master regulators targeting other transcription factors or other factors involved in chromatin state regulation. Only about 30% of the EIN3 binding sites were associated with transcriptional changes, but at least two-thirds were not (Figure 1D, Figure 1—figure supplement 2). EIN3 candidate targets that are not transcriptionally activated may require cofactors to induce a change in expression for a specific environmental response or developmental program. Quantitatively, the changes in EIN3 binding and steady-state transcription upon ethylene treatment do not correlate because the temporal transcription patterns are very diverse (Figure 2—figure supplement 1). However, relatively high levels of EIN3 occupancy in etiolated seedlings treated with ethylene indeed correspond to increases in steady-state levels of transcription (Figure 2A). In fact, we were able to differentiate the characteristics of EIN3 candidate targets that exhibited a transcriptional response to ethylene from those that do not (Figure 2A). EIN3 candidate targets that exhibit increased occupancy and increased levels of transcription (EIN3-R) are functional targets, enriched in gene families with specific functions, for example BZR, TIFY, and bHLH transcription factor families, which play a role in other hormone pathways (p<0.05) (Figure 2B). The highest percentage of hormone-associated genes occurs in EIN3 candidate targets that are ethylene-regulated (EIN3-R) (Figure 2B, inset), and it is likely that these EIN3-R targets are direct and/or functional. Other EIN3 candidate targets may play roles in different developmental stages/tissue types, or may be under spatial regulation, requiring specific cofactors. Figure 2 with 3 supplements see all Download asset Open asset The ethylene transcriptional response occurs in four distinct waves of transcriptional induction. (A) Ethylene-regulated EIN3 targets (EIN3-R) exhibit increased binding at transcription start sites (TSS) upon ethylene treatment (black arrows) in comparison to those not transcriptionally regulated by ethylene (EIN3-NR and EIN3-ND). Each boxplot represents the distribution of EIN3 ChIP-Seq RPKMs near the TSS. (B) Distribution of gene families among EIN3-R targets reveals over-representation of gene families related to hormone responses function. (Inset) Percentage of hormone-related genes in EIN3 binding and transcription categories. (C) DREM paths representing waves of induction of steady-state levels of transcription by ethylene for genes that are regulated by EIN3, implicating different modes of transcriptional regulation in the ethylene response. Right panels contain all genes for each wave. https://doi.org/10.7554/eLife.00675.009 Projection of the dynamic EIN3 binding (ChIP-Seq) onto the transcriptional ethylene response (mRNA-Seq) using the Dynamic Regulatory Events Miner (DREM) (Ernst et al., 2007) revealed that the ethylene response occurs in four waves of transcription significantly regulated by EIN3 (Pathway hypergeometric p<10−10) (Figure 2C). These waves display distinct temporal transcription behaviors (Hypergeometric p<0.001), and the reduction of transcriptional noise occurs in successive temporal waves (Figure 2C, Figure 2—figure supplement 2). Genes that were enriched in specific biological functions within these four transcriptional waves include RNA binding/translation (Wave 1, Wave 3), cell wall maintenance (Wave 2), and response to endogenous stimulus (Wave 4). The second wave is also enriched for genes involved in cell wall maintenance, and the expression of these genes steadily increases following 1 hr of ethylene treatment, consistent with kinetics of EIN3-dependent growth inhibition (Binder et al., 2004a; Vandenbussche et al., 2012). The four waves of the ethylene transcriptional response each contain a unique subset of EIN3 candidate targets. The first wave is highly variable, lower in steady-state levels of transcription, and it also contains the lowest percentage of EIN3 candidate targets and hormone-related genes (Figure 2C). Previous ethylene growth rate inhibition studies have shown that low amounts of ethylene can result in adaptation and desensitization to subsequent ethylene stimulation (Binder et al., 2004a, 2004b) . This first wave may serve as the immediate ethylene response, activating initial ethylene response genes as well as those that serve to desensitize the plant to subsequent ethylene stimulation, but this has yet to be shown. The next three waves of transcription are successively less variable and contain higher percentages of EIN3 candidate targets and hormone-related genes. The four waves of ethylene-induced transcription account for 50% of the transcriptionally ethylene-regulated EIN3 targets (EIN3-R), and the remaining EIN3 candidate targets are distributed among other patterns of transcription that do not contain significant numbers of EIN3 candidate targets in each transcriptional trajectory (Pathway hypergeometric p<10−10) (Figure 2—figure supplement 3). The expression kinetics and reduction of transcriptional noise we observe in the ethylene-induced waves may be tied to distinct mechanisms of transcriptional control, or they may reflect heterogeneity of the ethylene response in different tissues, which can be resolved using single cell analysis. From the temporal ethylene transcriptional response patterns, it appears that the initial early ethylene transcriptional response is noisy and less focused functionally. During sustained exogenous ethylene application, EIN3 accumulates, and the established ethylene transcriptional response is hormone-focused and less noisy, but feed-forward and feed-back mechanisms mentioned below may serve to establish this functional specificity. A recurring theme throughout this study is that the key players in the ethylene transcriptional response regulated by EIN3 are involved in plant hormone response pathways, and we anticipate a dense network of interconnections between the coregulated hormone pathways because hormones operate in concert, synergistically/antagonistically regulating growth and development. Although hormone pathway interconnections have been previously described by many groups (Kaufmann et al., 2009, 2010; Sun et al., 2010; Yu et al., 2011), here we show that these interconnections exist at many regulatory levels and that the targets of EIN3 may regulate genes in these responses. Among the EIN3 candidate targets, we observed the enrichment of hormone-related targets among many different categorical sets (Figure 2B, inset). These EIN3 targets include downstream effectors of the ethylene response, key ethylene signaling players, and genes involved in other hormone pathways/responses. Many of the EIN3-modulated downstream effectors are members of the AP2/ERF transcription factor family, and as expected, these transcriptional initiators are up-regulated by ethylene (Figure 3A, inset, green font). Figure 3 with 1 supplement see all Download asset Open asset Functional classification of EIN3 candidate targets reveals genes involved in hormone responses. (A) Feedback (ethylene signaling components, above) of the ethylene response and feedforward (downstream effectors, below). Downstream effectors in green are transcriptionally induced by ethylene. Known EIN3 targets are noted by asterisks; all other EIN3 candidate targets were discovered by this study. (B and C) EIN3 candidate targets are involved in hormone co-regulation. Node color represents hormone annotation, as indicated in B; large nodes are EIN3 candidate targets. Dark grey edges represent protein-protein interactions (PPI) and light grey edges are protein–DNA interactions (PDI). Hormone annotation legend: abscisic acid (ABA), brassinosteroid (BR), cytokinin (CK), ethylene (ETH), gibberellin (GA), auxin (IAA), methyl jasmonate (MJ), salicylic acid (SA), >1, more than one hormone. (D) EIN3-mediated ethylene co-regulation occurs at many different levels. PPIs are from the Arabidopsis Interactome Mapping Consortium, and EIN3 PDIs are from this study. https://doi.org/10.7554/eLife.00675.013 Given that EIN3, the master regulator of the ethylene transcriptional response, acts at the culmination of the ethylene signal transduction pathway and is the transcriptional initiator of the ethylene response, one would expect a large number of downstream effectors to coordinate the transcriptional cascade and feedback regulators to maintain the circuitry in a homeostatic state as opposed to a feed-forward runaway response. Analysis of the ethylene-regulated EIN3 targets reveals a number of sites of ethylene signaling modulation of which the majority are negative regulators, supporting the idea that EIN3 is at the end of a signal transduction pathway, and that this regulatory logic dictates a negative feedback loop for homeostatic adaptable systems. More specifically, several negative regulators of the ethylene signaling pathway (Kendrick and Chang, 2008) were targets of EIN3 (Figure 3A), including three ethylene receptors (ETHYLENE RESPONSE2 [ETR2], ETHYLENE RESPONSE SENSOR1/2 [ERS1/2]), as well as REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1), CONSTITUTIVE TRIPLE RESPONSE1 (CTR1), and the previously mentioned EBF1/2. The induction of ETR2, ERS1/2 by ethylene was previously reported and has been suggested to restore ethylene receptor activity, resensitizing the plant to ethylene (Binder et al., 2004b; Vandenbussche et al., 2012). The negative regulation of ethylene signaling by EIN3 through induction of CTR1 and ETR2 is further supported by the literature (Chen et al., 2007), suggesting that these proteins exhibit an increase in stabilization upon ethylene treatment (Gao et al., 2003). The EIN3 candidate targets account for more than twice the proportion of hormone genes than in the genome (46%, Hypergeometric p=10−96) (Figure 2B, inset) (Alonso et al., 2003a; Nemhauser et al., 2006; Peng et al., 2008). Many of the genes were involved in more than one hormone response, highlighting the extensive hormone co-regulation in Arabidopsis (Figure 3B). Hormone co-regulation is evident in the protein-protein as well as the transcriptional regulator interactions and this network reveals interconnectivity suggestive of robust regulatory co-regulation (Figure 3C). Many detailed examples of hormone co-regulation exist in the literature, but often the mechanism(s) of co-regulation is unknown. Previous ChIP-chip or ChIP-Seq studies from plants have also revealed cross-regulation within pathways involved in flowering and in roots (Yant et al., 2010; Iyer-Pascuzzi et al., 2011; Winter et al., 2011; Immink et al., 2012) . The findings presented in our study suggest that (1) hormone co-regulation can occur through the binding of EIN3, (2) EIN3 targets hormone pathways at multiple levels, and (3) some of these events are transcriptionally regulated by ethylene (Figure 3D). Ethylene and jasmonate co-regulation occurs at the transcriptional level, sharing a complement of genes responsive to both hormones, for example RAP2.6L, ERF1. EIN3 also targets four JAZ repressors, two of which are transcriptionally regulated by ethylene (JAZ1, JAZ6). In general, ethylene and jasmonate are known to function synergistically and in the presence of jasmonate, JAZ1 proteins bound to EIN3 are degraded, relieving the EIN3 transcriptional activation (Zhu et al., 2011). Here, the presence of an exogenous ethylene stimulus primes cells for a jasmonate response, by loading the promoters of jasmonate/ethylene response genes with EIN3 and JAZ proteins, poising the plant for a jasmonate-ethylene driven transcriptional program, as required for plant pathogen response. Reports of anticipatory binding in other organisms have been forth coming (Macquarrie et al., 2011; Lickwar et al., 2012). Ethylene and gibberellin co-regulation through EIN3 occurs at signal reception (GID1B, GID1C) and transcription (PIF3). The regulatory logic of EIN3 binding results in an up-regulation of the gibberellin response; GID receptors target DELLA repressors for degradation, which releases PIF3 from repression, resulting in the activation of the gibberellin transcriptional response. Additional support for feed-forward transcription is provided by over-representation of the PIF3 motif in the promoter sequences of the ethylene transcriptional response genes (Supplementary file 1E, Figure 3—figure supplement 1). Hormone co-regulation may also occur bidirectionally as a recent study reported negative regulation of ethylene by FUSCA3 (FUS3), known to regulate and be regulated by gibberellin and abscisic acid in embryonic and vegetative timing (Lumba et al., 2012). FUS3 negatively regulates genes upstream and downstream of EIN3 (EIN2 and ERF1) in leaf aging (Lumba et al., 2012). Ethylene and auxin co-regulation occurs at both the level of transport and transcriptional response, as EIN3 modulates a regulator of auxin efflux (PID) and its upstream activator (PBP1), and at least seven auxin response proteins (Supplementary file 1B). EIN3 also targets the auxin transporter (AUX1) and an auxin signaling gene (IAA29), but these candidate targets are not responsive to ethylene in etiolated seedlings (Supplementary file 1B). Ethylene has been reported to stimulate auxin transport through AUX1 away from the root apex, to decrease lateral root primordia (Lewis et al., 2011). Therefore, it is likely these binding events have functional outcomes in specific tissue types or developmental programs not addressed in this study. The establishment of a transcriptional program tailored to result in a specific growth and development process requires multiple levels of transcriptional modulation. EIN3 was previously suggested to initiate a transcriptional cascade because it activates AP2/ERF transcription factors ERF1/EDF1 (Solano et al., 1998). To determine additional candidate downstream effectors that may modulate the ethylene transcriptional response cascade, we used in vitro protein binding microarrays to generate DNA-binding motifs for 12 transcription factors that were ethylene-regulated targets of EIN3 (see ‘Materials and methods’). We then used the in vitro DNA-binding motifs to scan the promoter sequences of all ethylene transcriptional response genes (Lam et al., 2011). EIN3 targets that may regulate a secondary transcriptional ethylene response include AP2/ERFs AT-ERF1, ERF5, and WRKY14/47, PIF3, NAC6, and RAP2.2, and the DNA-binding motifs of the aforementioned transcription factors are over-represented in the promoter regions of genes that are regulated by ethylene (Hypergeometric p<10−5) (Supplementary file 1E, Figure 3—figure supplement 1). Future in vivo analyses of the targets of these transcription factors may help elucidate their contribution to the transcriptional cascade of the ethylene response. The extensive hormone co-regulation that occurs in waves of transcription leads to certain testable predictions regarding the key regulatory hubs and transcriptional cascades at a genome-wide level. Using a global approach, we are able to determine not only if one gene is a candidate target of EIN3, but whether its homologs are targets as well. Transcription factor targeting of genes that are homologous, with overlapping and unique functions, can add diversity to the outputs of transcriptional programs (Macquarrie et al., 2011). One of the most striking and surprising example we found was the direct regulation of the three homologs by EIN3, HOOKLESS1 (HLS1) and HLS1-LIKE HOMOLOG2 (HLH2), and to a lesser extent HLH1 (Figure 4A, HLH1 in Figure 4—figure supplement 1). This led us to experimentally test the functionality of all four members of the HLS1 gene family in etiolated seedling growth and development. HLS1 is a well-known signal integrator of ethylene, light, auxin, sugar, and brassinolide (de Grauwe et al., 2005; Hou et al., 1993; Li et al., 2004; Ohto et al., 2006) and was previously hypothesized to be a target of ERF1 because of the presence of a GCC box motif in the HLS1 promoter region sequence (Lehman et al., 1996). The binding of EIN3 to the promoters of HLS1, HLH2, and HLH1 increased upon ethylene treatment (Figure 4—figure supplement 1) and is specific to EIN3 (Figure 4B). The EIN3 binding sites in these promoters contain known EIN3 motifs (Figure 4—figure supplement 1). The functional significance of the HLS1 EIN3 binding site is supported by a previous study that identified two allelic mutations in the HLS1 promoter sufficient to yield a ‘hookless’ phenotype (Lehman et al., 1996). Previous studies have also shown that ein2 is deficient in the accumulation of EIN3 protein (Guo and Ecker, 2003) and HLS1 mRNA, (Lehman et al., 1996). We also observed HLS1 steady-state transcript levels were significantly reduced in the ein3-1 eil1-1 mutant (Figure 4—figure supplement 2). Figure 4 with 4 supplements see all Download asset Open asset EIN3 binding facilitates HLS1 ethylene-auxin hormone co-regulation. (A) (Top panel) EIN3 targets HLS1 and HLH2. Temporal EIN3 binding and expression patterns are shown with known EIN3 targets as a control. HLH1 and HLH3 are not expressed in etiolated seedlings. (B) Binding of EIN3 to HLS1/HLH2 promoters is dependent on presence of EIN3. (C)–(F) Mutations in HLS1 and its homologs reveal severe growth and developmental defects. (C) Tri-cotyledon phenotypes in apical hook of quadruple mutants. Images were taken at the same magnification. (D) HLS1 gene family has a role in embryo patterning. SEM image scale bar, 50 μm. (E) Adult three-week-old plants displayed dwarfed phenotypes similar to axr1. (F) Quadruple mutants display floral defects similar to arf3/ettin. Inset and panels on the right show abnormal guard cell patterning. SEM scale bars, 100 μm. https://doi.org/10.7554/eLife.00675.015 Ethylene and auxin co-regulate plant growth and development and it is likely that this co-regulation is mediated in part by EIN3 regulation of HLS1/HLHs. To understand this hormone co-regulation, we generated quadruple mutants for the HLS1 gene family and also further characterized their role as regulatory hub signal integrators (Figure 4—figure supplement 3). The pleiotropic phenotypes we observed support the role of the HLS1 gene family in auxin regulated plant growth and development (Figure 4C–F). We observed severe defects in the embryonic patterning, etiolated seedlings, adult plant morphology, and floral morphology. The adult quadruple mutants display a dwarf phenotype, similar to the auxin mutant axr1 (Leyser et al., 1993), and floral morphology of the quadruple mutants display two stigmas atop a gynoecium, similar to the arf3/ettin mutant floral phenotype (Sessions and Zambryski, 1995). Although HLS1 is known to be involved in the differential growth of the apical hook and is necessary for the accumulation of AUXIN RESPONSE FACTOR2 (ARF2) DNA-binding protein (Li et al., 2004; Ohto et al., 2006), the biochemical function of these putative N-acetyltransferases remains to be determined. Using a genome-wide approach, we found that not only HLS1, but other gene family members are targets of EIN3 and that the requirement of the HLS proteins for hormone responses extends beyond apical hook development to many other processes from embryo patterning to flowering, linking the regulation of growth and development by ethylene to many new biological processes in novel ways. Discussion To date, few temporal transcription factor binding studies have been undertaken (Hiroi, 2004; Ni et al., 2009; Zinzen et al., 2009). Temporal protein–DNA interactions are often difficult to reconcile with gene expression profiles and the complexity of regulation that occurs transcriptionally is very challenging to characterize and interpret biologically. Here, by jointly analyzing the temporal expression and genome-wide binding data of one key transcription factor in response to hormone stimulus, we were able to reveal several important properties of the hormone responsive transcriptional program and identify new components in the signaling pathway. We found that upon a timecourse of ethylene treatment, EIN3 binding was induced, resulting in various transcriptional patterns and that the ethylene transcriptional response occurred in waves of transcription that were temporally distinct and could be attributed to different biological functions, variable in the amount of noise, and significantly regulated by EIN3. EIN3 modulated genes were over-represented in hormone co-regulation, and the specific targets in the other hormone pathways, as reported in this study, suggest these ‘cross-talk’ events may involve multiple levels of regulation. Interestingly, feedback regulation of the ethylene response by EIN3 enabled the ide" @default.
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W4230615659 title "Decision letter: Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis" @default.
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