The Most Deeply Conserved Noncoding Sequences in Plants Serve Similar Functions to Those in Vertebrates Despite Large Differences in Evolutionary Rates

Burgess, Diane; Freeling, Michael

doi:10.1105/tpc.113.121905

Cited by 38 publications

(28 citation statements)

References 99 publications

(129 reference statements)

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“…We found that CNSs were enriched for TF bound regions compared with randomly selected regions for six out of eight data sets, illustrating the functional regulatory character of these sequences. Furthermore, using a more extended phylogenetic sampling than used in previous research (Burgess and Freeling, 2014), we were able to discover 715 TFBSs for 501 genes that were conserved from dicots to Viridiplantae. Functions associated with this gene set comprise basal biological processes such as transport, carbohydrate metabolism, and cell cycle.…”

Section: Discussionmentioning

confidence: 93%

“…The authors discovered that, based on 10 species, a subset of 37 CNSs could be found in all flowering plants. The detected CNSs were functionally similar to vertebrate CNSs, being highly associated with TF-encoding and developmental genes and also enriched in TFBSs (Burgess and Freeling, 2014).…”

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confidence: 78%

“…A pioneering study in plant CNS research suggests that CNSs in grasses (plants) are smaller and far less frequent than those identified in mammalian genes (Kaplinsky et al, 2002). A recent attempt to identify very deeply conserved CNSs reported that sequences conserved throughout the Eudicot clade of flowering plants could be detected (Burgess and Freeling, 2014). The authors discovered that, based on 10 species, a subset of 37 CNSs could be found in all flowering plants.…”

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confidence: 99%

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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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Section: Discussionmentioning

confidence: 93%

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confidence: 78%

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confidence: 99%

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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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“…Similarly, NCARs showed a clustering pattern (Figs. 2b, S2, Table S3) that is also typical of conserved non-coding elements in mammals [42] and plants [53]. All NCARs contained 56.6% AT on average, compared to the mean genomic background of 61.8% AT (Table S4).…”

Section: The Conserved Regulatory Landscape Of Beesmentioning

confidence: 95%

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Jones

Hunt

et al. 2018

Preprint

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14The evolutionary origins of eusociality represent increases in complexity from individual to caste-15 based, group reproduction. These behavioral transitions have been hypothesized to go hand-in- 16hand with an increased ability to regulate when and where genes are expressed. Bees have 17 convergently evolved eusociality up to five times, providing a framework to test this hypothesis. 18To examine potential links between putative gene regulatory elements and social evolution, we 19 compare alignable, non-coding sequences in eleven diverse bee species, encompassing three 20 independent origins of reproductive division of labor and two elaborations of eusocial complexity. 21We find that rates of evolution in a number of non-coding sequences correlate with key social 22 transitions in bees. Interestingly, while we find little evidence for convergent rate changes 23 associated with independent origins of social behavior, a number of molecular pathways exhibit 24 convergent rate changes in conjunction with subsequent elaborations of social organization. We 25 also present evidence that many novel non-coding regions may have been recruited alongside 26 the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements 27 associated with division of labor within this group. Thus, our findings are consistent with the 28 hypothesis that gene regulatory innovations are associated with the evolution of eusociality and 29 illustrate how a thorough examination of both coding and non-coding sequence can provide a 30 more complete understanding of the molecular mechanisms underlying behavioral evolution. 32 33Introduction 34 35Many genomic sequences that do not encode proteins play essential roles in gene regulation 36 across animals [1] and plants [2]. The breadth of knowledge of these non-coding regulatory 37 elements has been built primarily upon the large number of plant and vertebrate genomes that 38 have been sequenced over the past decade. However, the high degree of conservation that exists 39 in a subset of these non-coding regions [1,3] means that comparative methods can be used to 40 identify similar non-coding elements even in the recently sequenced genomes of non-model taxa 41 that frequently lack the resources needed to characterize regulatory regions via functional assays. outside of Drosophila [4], the non-coding regulatory landscape of these taxa has been the target 44 of few studies. 46Here, we take advantage of eleven publicly-available bee genomes [5][6][7][8][9] to examine how non-47 coding elements change as eusociality -an extreme form of social behavior found primarily in 48 insects and mammals -has convergently evolved and increased in complexity within bees. 49Eusociality is of particular interest to evolutionary biologists because it represents an increase in 50 complexity from individual to group-level reproduction and includes the evolution of a non-51 reproductive worker caste [10]. Along with reproductively-specialized castes, many of these 52 societies have also e...

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“…Thus, some genes are present in all eukaryotes, whereas others may be lineage specific (21) . Equivalently, a subset of CNS identified across Brassicaceae (1) are identifiable across all surveyed angiosperms including Amborella (2) whereas others are uniquely shared by only a subset of Brassicaceae.…”

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confidence: 96%

Evolution of conserved noncoding sequences in Arabidopsis thaliana

Yocca

Schmitz

et al. 2019

Preprint

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Recent pangenome studies have revealed a large fraction of the gene content within a species exhibits presence-absence variation (PAV). However, coding regions alone provide an incomplete assessment of functional genomic sequence variation at the species level. Little to no attention has been paid to noncoding regulatory regions in pangenome studies, though these sequences directly modulate gene expression and phenotype. To uncover regulatory genetic variation, we generated chromosome-scale genome assemblies for thirty Arabidopsis thaliana accessions from multiple distinct habitats and characterized species level variation in Conserved Noncoding Sequences (CNS). Our analyses uncovered not only evidence for PAV and positional variation (PosV) but that diversity in CNS is non-random, with variants shared across different accessions. Using evolutionary analyses and chromatin accessibility data, we provide further evidence supporting roles for conserved and variable CNS in gene regulation. Characterizing species-level diversity in all functional genomic sequences may later uncover previously unknown mechanistic links between genotype and phenotype. Introduction:Conserved noncoding DNA remains a highly understudied class of functional genomic features compared to protein-coding genes. Previous comparative genomic analyses in plants have identified stretches, generally 15-150 base pairs (bp) long ( Fig S1), of noncoding regions that are positionally-conserved with identical (or near identical) sequence across distantly related species (1-4) .These sequences, commonly referred to as Conserved Noncoding Sequences (CNS), are regions in the genome displaying much higher similarity across different taxa than expected by chance. Background mutation and genetic drift purges non-functional sequences over long evolutionary distances. Therefore, sequence conservation above expectation implies purifying selection actively conserves these CNS. Indeed, Williamson et al. (5) discovered elevated signatures of purifying selection in CNS regions compared to other classes of noncoding DNA in Capsella grandiflora . Previous studies demonstrated CNS contain transcription factor binding sites (TFBS) (2, 6, 7) .TFBS are typically 6-12 base-pair (bp) long (8) . CNS can exceed this length, as they are thought to consist of arrays of TFBS capable of recruiting independent or cooperative transcriptional protein complexes. The length of CNS enables high confidence identification of orthologous cis-regulatory elements in comparator genomes. Querying genomes for TFBS alone results in a high false positive rate, as there are >30,000 expected occurrences of a given six bp sequence expected by chance even in the relatively small (~135 Mb) Arabidopsis thaliana genome. In contrast, there is less than one expected

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The Most Deeply Conserved Noncoding Sequences in Plants Serve Similar Functions to Those in Vertebrates Despite Large Differences in Evolutionary Rates

Cited by 38 publications

References 99 publications

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

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

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Evolution of conserved noncoding sequences in Arabidopsis thaliana

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