The prevalence, evolution and chromatin signatures of plant regulatory elements

Lu, Zefu; Marand, Alexandre P.; Ricci, William A.; Ethridge, Christina L; Zhang, Xiaoyu; Schmitz, Robert J.

doi:10.1038/s41477-019-0548-z

Cited by 274 publications

(387 citation statements)

References 86 publications

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“…random occurrence of the shortest CNS (15bp). TFBS colocalize with accessible chromatin in mammalian genomes, as do CNS as demonstrated previously in plants (4,(9)(10)(11)(12)(13)(14) .…”

supporting

confidence: 78%

“…Strong evidence of CNS overlapping signatures of accessible chromatin has been reported previously (6,(9)(10)(11)13) . In each case, the set of CNS queried was different, with estimates ranging from observed here.…”

Section: Are Variable Cns Associated With Accessible Chromatin?supporting

confidence: 68%

“…Future studies are needed to test whether PosV CNS sites are associated with regions of higher recombination. Second, the movement of regulatory elements may involve transposable elements (TEs) as shown previously (13,(44)(45)(46) . Indeed, we observe strong bias with respect to the colocalization of PosV CNS and TEs relative to collinear CNS ( Fig S13; Fig S15).…”

Section: Are There Relationships Between Cns Class and Transposable Ementioning

confidence: 94%

“…We performed Assay for Transposase-Accessible Chromatin sequencing (ATAC-seq) in leaf tissue for eighteen accessions, including the reference accession Col-0. This method identifies genomic regions accessible by a Tn5 transposase, and such regions of accessible chromatin are often associated with cis -regulatory DNA elements and transcription factor binding (13,14,34) . We utilized a protocol which combines fluorescence-activated nuclei sorting and ATAC-seq (FANS-ATAC-seq; 12) .…”

Section: Are Variable Cns Associated With Accessible Chromatin?mentioning

confidence: 99%

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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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“…random occurrence of the shortest CNS (15bp). TFBS colocalize with accessible chromatin in mammalian genomes, as do CNS as demonstrated previously in plants (4,(9)(10)(11)(12)(13)(14) .…”

supporting

confidence: 78%

Section: Are Variable Cns Associated With Accessible Chromatin?supporting

confidence: 68%

Section: Are There Relationships Between Cns Class and Transposable Ementioning

confidence: 94%

Section: Are Variable Cns Associated With Accessible Chromatin?mentioning

confidence: 99%

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Evolution of conserved noncoding sequences in Arabidopsis thaliana

Yocca

Schmitz

et al. 2019

Preprint

Self Cite

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“…While DNA methylation in P. patens is mostly targeted to TEs, transposon methylation could influence the expression of nearby genes 31,32 . In comparison to TEs, where internal methylation auto-silencing the elements, in genes methylation commonly regulates expression (activation and suppression) by targeting external-genic elements [33][34][35][36][37][38] . Additionally, genetic interaction networks are more robust in genes than in transposons.…”

Section: Complementation and Superiority Of Non-cg Methylation Over Cmentioning

confidence: 99%

Non-CG methylation is superior to CG methylation in genome regulation

Domb

Katz

Yaari

et al. 2020

Preprint

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DNA methylation in plants occurs in CG, CHG, and CHH sites. While depletion of CG methylation in transposons is associated with ample transcriptional activation, it was mainly studied in species with limited non-CG methylation that is linked to CG methylation. Here we profiled transcription in the moss plant, Physcomitrella patens, that has robust non-CG methylation with similar symmetrical CG and CHG methylation levels. Separated contextual methylation mechanisms in Physcomitrella patens enabled generation of numerous contextspecific hypomethylated mutants. Our transcriptome data show that specific elimination of CG methylation is fully complemented by non-CG methylation. Conversely, exclusive removal of non-CG methylation massively dysregulated genes and transposons. Moreover, CHG methylation silenced transposons stronger than CG methylation. Lastly, we found non-CG methylation as crucial for silencing CG-depleted transposons. These results demonstrate the potency of non-CG methylation in genome regulation and suggest that it evolved due to moderate silencing and/or rapid mutability of methylated CGs.

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Regulatory dynamics distinguishing desiccation tolerance strategies within resurrection grasses

et al. 2022

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Desiccation tolerance has evolved recurrently in grasses using two unique strategies of either protecting or dismantling the photosynthetic apparatus to minimize photooxidative damage under life without water (anhydrobiosis). Here, we surveyed chromatin architecture and gene expression during desiccation in two closely related grasses with distinguishing desiccation tolerance strategies to identify regulatory dynamics underlying these unique adaptations. In both grasses, we observed a strong association between nearby chromatin accessibility and gene expression in desiccated tissues compared to well‐watered, reflecting an unusual chromatin stability under anhydrobiosis. Integration of chromatin accessibility (ATACseq) and expression data (RNAseq) revealed a core desiccation response across these two grasses. This includes many genes with binding sites for the core seed development transcription factor ABI5, supporting the long‐standing hypothesis that vegetative desiccation tolerance evolved from rewiring seed pathways. Oropetium thomaeum has a unique set of desiccation induced genes and regulatory elements associated with photoprotection, pigment biosynthesis, and response to high light, reflecting its adaptation of protecting the photosynthetic apparatus under desiccation (homoiochlorophyly). By contrast, Eragrostis nindensis has unique accessible and expressed genes related to chlorophyll catabolism, scavenging of amino acids, and hypoxia, highlighting its poikilochlorophyllous adaptations of dismantling the photosynthetic apparatus and degrading chlorophyll under desiccation. Together, our results highlight the complex regulatory and expression dynamics underlying desiccation tolerance in grasses.

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The prevalence, evolution and chromatin signatures of plant regulatory elements

Cited by 274 publications

References 86 publications

Evolution of conserved noncoding sequences in Arabidopsis thaliana

Evolution of conserved noncoding sequences in Arabidopsis thaliana

Non-CG methylation is superior to CG methylation in genome regulation

Regulatory dynamics distinguishing desiccation tolerance strategies within resurrection grasses

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