A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in<i>Arabidopsis thaliana</i>

Lindemose, Søren; Jensen, Michael K.; Velde, Jan Van de; O'Shea, Charlotte; Heyndrickx, Ken S.; Workman, Christopher T.; Vandepoele, Klaas; Skriver, Karen; Masi, Federico De

doi:10.1093/nar/gku502

Cited by 85 publications

(76 citation statements)

References 67 publications

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“…ABF3 is a bZIP master regulator of ABA signaling that controls ABRE-dependent gene expression (16), GBF3 is a bZIP factor that binds G-box motifs (25), and AFP3 interacts with the bZIP protein ABI5 to fine-tune the ABA response (24). NAP, an NAC TF associated with stress and senescence (26,27), controls the expression of ABSCISIC ALDEHYDE OXIDASE3 (AAO3), an enzyme that catalyzes the final steps of ABA synthesis (28), and thereby may contribute further to ABA accumulation (Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

González-Grandío

Pajoro

Franco-Zorrilla

et al. 2016

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

243

239

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Shoot-branching patterns determine key aspects of plant life and are important targets for crop breeding. However, we are still largely ignorant of the genetic networks controlling locally the most important decision during branch development: whether the axillary bud, or branch primordium, grows out to give a lateral shoot or remains dormant. Here we show that, inside the buds, the TEOSINTE BRANCHED1, CYCLOIDEA, PCF (TCP) transcription factor BRANCHED1 (BRC1) binds to and positively regulates the transcription of three related Homeodomain leucine zipper protein (HD-ZIP)-encoding genes: HOMEOBOX PROTEIN 21 (HB21), HOMEOBOX PROTEIN 40 (HB40), and HOMEOBOX PROTEIN 53 (HB53). These three genes, together with BRC1, enhance 9-CIS-EPOXICAROTENOID DIOXIGENASE 3 (NCED3) expression, lead to abscisic acid accumulation, and trigger hormone response, thus causing suppression of bud development. This TCP/HD-ZIP genetic module seems to be conserved in dicot and monocotyledonous species to prevent branching under light-limiting conditions.

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Section: Discussionmentioning

confidence: 99%

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

González-Grandío

Pajoro

Franco-Zorrilla

et al. 2016

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

243

239

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“…This process of assigning functions to the predicted target genes proves useful for genes for which little functional information is available. Assessing the functional coherence of target genes is an alternative manner to validate regulatory interactions and is based on the idea that genes that are part of the same biological pathway are regulated by similar sets of TFs (Marbach et al, 2012;Lindemose et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

A Collection of Conserved Noncoding Sequences to Study Gene Regulation in Flowering Plants

Velde

Bel²,

Vaneechoutte³

et al. 2016

Plant Physiol.

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Transcription factors (TFs) regulate gene expression by binding cis-regulatory elements, of which the identification remains an ongoing challenge owing to the prevalence of large numbers of nonfunctional TF binding sites. Powerful comparative genomics methods, such as phylogenetic footprinting, can be used for the detection of conserved noncoding sequences (CNSs), which are functionally constrained and can greatly help in reducing the number of false-positive elements. In this study, we applied a phylogenetic footprinting approach for the identification of CNSs in 10 dicot plants, yielding 1,032,291 CNSs associated with 243,187 genes. To annotate CNSs with TF binding sites, we made use of binding site information for 642 TFs originating from 35 TF families in Arabidopsis (Arabidopsis thaliana). In three species, the identified CNSs were evaluated using TF chromatin immunoprecipitation sequencing data, resulting in significant overlap for the majority of data sets. To identify ultraconserved CNSs, we included genomes of additional plant families and identified 715 binding sites for 501 genes conserved in dicots, monocots, mosses, and green algae. Additionally, we found that genes that are part of conserved mini-regulons have a higher coherence in their expression profile than other divergent gene pairs. All identified CNSs were integrated in the PLAZA 3.0 Dicots comparative genomics platform (http://bioinformatics.psb.ugent.be/plaza/versions/plaza_v3_dicots/) together with new functionalities facilitating the exploration of conserved cis-regulatory elements and their associated genes. The availability of this data set in a user-friendly platform enables the exploration of functional noncoding DNA to study gene regulation in a variety of plant species, including crops.

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“…Therefore, as an alternative to using TF perturbation in a single condition, we sought potential target genes that show functional coherence, a sign of bona fide regulated genes. False positive potential target genes will not show functional coherence with other potential target genes, in contrast to genuine regulated genes (Lindemose et al, 2014). To delineate functionally coherent subsets of bound genes per TF, the enrichment of potential targets was determined in 1563 functional gene modules (Heyndrickx and Vandepoele, 2012).…”

Section: Construction Of An Experimental Arabidopsis Gene Regulatory mentioning

confidence: 99%

“…HOT regions show reduced p values compared with the non-HOT regions, which can be explained by the necessity to retain binding sites for more TFs than Because of their function, bound regions are also often conserved across species, which is the premise of genome-wide studies of conserved noncoding sequences (CNSs). We determined the fraction of bound regions exhibiting conservation within the crucifers (Haudry et al, 2013) and within the dicot lineage (Van de Velde et al, 2014) based on overlap with CNSs. Overall, CNSs supported 35 and 29% of the 24,898 bound regions in the crucifer and dicot data, and 15% are supported in both sets.…”

Section: Population Sequence Diversity and Conservation Of Bound Dnamentioning

confidence: 99%

“…The chromatin states were downloaded from Supplemental Data Set 2 from SequeiraMendes et al (2014). The CNS data in dicots and crucifers was taken from Van de Velde et al (2014) and Haudry et al (2013), respectively. The HOT and non-HOT-bound region files of each TF were formatted as BED files.…”

Section: Enrichment Analysis Of Bound Regions In Different Genomic Rementioning

confidence: 99%

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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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A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors inArabidopsis thaliana

Cited by 85 publications

References 67 publications

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

A Collection of Conserved Noncoding Sequences to Study Gene Regulation in Flowering Plants

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

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