An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions

Haudry, Annabelle; Platts, Adrian E.; Vello, Emilio; Hoen, Douglas R.; Leclercq, Mickaël; Williamson, R.; Forczek, Ewa; Joly‐Lopez, Zoé; Steffen, Joshua G.; Hazzouri, Khaled M.; Dewar, Ken; Stinchcombe, John R.; Schoen, Daniel J.; Wang, Xiaowu; Schmutz, Jeremy; Town, Christopher D.; Edger, Patrick P.; Pires, J. Chris; Schumaker, Karen S.; Jarvis, David E.; Mandáková, Terezie; Lysak, Martin A.; Bergh, Erik van den; Schranz, M. Eric; Harrison, Paul M.; Moses, Alan M.; Bureau, Thomas E.; Wright, Stephen I.; Blanchette, Mathieu

doi:10.1038/ng.2684

Cited by 348 publications

(462 citation statements)

References 94 publications

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“…In comparison with coding genes, the noncoding part of diatom genomes remains vastly unexplored, with no precise information on noncoding regions that might act as regulatory elements, as reported in animals, plants and unicellular eukaryotes (Vavouri et al ., 2007; Piganeau et al ., 2009; Haudry et al ., 2013). Here, we take a first step towards the identification and classification of CNEs in diatoms using a comparative genomic approach centred on P. multistriata .…”

Section: Resultsmentioning

confidence: 99%

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

et al. 2017

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Summary Microalgae play a major role as primary producers in aquatic ecosystems. Cell signalling regulates their interactions with the environment and other organisms, yet this process in phytoplankton is poorly defined. Using the marine planktonic diatom Pseudo‐nitzschia multistriata, we investigated the cell response to cues released during sexual reproduction, an event that demands strong regulatory mechanisms and impacts on population dynamics.We sequenced the genome of P. multistriata and performed phylogenomic and transcriptomic analyses, which allowed the definition of gene gains and losses, horizontal gene transfers, conservation and evolutionary rate of sex‐related genes. We also identified a small number of conserved noncoding elements.Sexual reproduction impacted on cell cycle progression and induced an asymmetric response of the opposite mating types. G protein‐coupled receptors and cyclic guanosine monophosphate (cGMP) are implicated in the response to sexual cues, which overall entails a modulation of cell cycle, meiosis‐related and nutrient transporter genes, suggesting a fine control of nutrient uptake even under nutrient‐replete conditions.The controllable life cycle and the genome sequence of P. multistriata allow the reconstruction of changes occurring in diatoms in a key phase of their life cycle, providing hints on the evolution and putative function of their genes and empowering studies on sexual reproduction.

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Section: Resultsmentioning

confidence: 99%

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

et al. 2017

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“…At the family level, motif clusters from the large and functionally diverse bZIP ( Figure 3A) and NAC families ( Figure S2B) closely reflected TF phylogeny (Corrêa et al, 2008;Olsen et al, 2005), indicating target sequences are conserved for close paralogs. Binding peaks of these TFs showed a range of enrichment in conserved non-coding regions (Haudry et al, 2013) (Figure S2C). Although the 529 DAP-seq motifs provided a global description of motif types, it was biased toward larger and more tractable families, such as bZIP, NAC, and WRKY, while some families, such as MADS and C3H, were underrepresented ( Figure S1A).…”

Section: The Arabidopsis Cistromementioning

confidence: 99%

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

O’Malley¹,

Huang²,

Song³

et al. 2016

Cell

373

482

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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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“…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%

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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An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions

Cited by 348 publications

References 94 publications

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

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

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