Enhancers associated with unstable RNAs are rare in plants

Mcdonald, Bayley R.; Picard, Colette; Brabb, Ian M.; Savenkova, Marina I.; Schmitz, Robert J.; Jacobsen, Steven E.; Duttke, Sascha H.

doi:10.1101/2023.09.25.559415

Cited by 3 publications

(3 citation statements)

References 78 publications

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“…Despite these similarities, enhancers in plants and animals differ in their histone modifications ( Lu et al 2019 ; Yan et al 2019 ; Silver et al 2023 ). The absence in plants of the canonical histone modifications that mark active enhancers in animals is consistent with the absence in plants of the bi-directional, short-lived enhancer RNAs found in animals ( Erhard et al 2015 ; Hetzel et al 2016 ; Thieffry et al 2020 ; Mcdonald et al 2023 ; Silver et al 2023 ). Thus, plants appear to use different mechanisms than animals for maintaining enhancer activity.…”

Section: Introductionsupporting

confidence: 75%

Plant enhancers exhibit both cooperative and additive interactions among their functional elements

Jores,

Tonnies,

Mueth

et al. 2024

The Plant Cell

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Enhancers are cis-regulatory elements that shape gene expression in response to numerous developmental and environmental cues. In animals, several models have been proposed to explain how enhancers integrate the activity of multiple transcription factors. However, it remains largely unclear how plant enhancers integrate transcription factor activity. Here, we use Plant STARR-seq to characterize three light-responsive plant enhancers—AB80, Cab-1, and rbcS-E9—derived from genes associated with photosynthesis. Saturation mutagenesis revealed mutations, many of which clustered in short regions, that strongly reduced enhancer activity in the light, in the dark or in both conditions. When tested in the light, these mutation-sensitive regions did not function on their own; rather, cooperative interactions with other such regions were required for full activity. Epistatic interactions occurred between mutations in adjacent mutation-sensitive regions, and the spacing and order of mutation-sensitive regions in synthetic enhancers affected enhancer activity. In contrast, when tested in the dark, mutation-sensitive regions acted independently and additively in conferring enhancer activity. Taken together, this work demonstrates that plant enhancers show evidence for both cooperative and additive interactions among their functional elements. This knowledge can be harnessed to design strong, condition-specific synthetic enhancers.

show abstract

Section: Introductionsupporting

confidence: 75%

Plant enhancers exhibit both cooperative and additive interactions among their functional elements

Jores,

Tonnies,

Mueth

et al. 2024

The Plant Cell

View full text Add to dashboard Cite

show abstract

“…Despite these similarities, enhancers in plants and animals differ in their histone modifications (Lu et al, 2019; Yan et al, 2019; Silver et al, 2023). The absence in plants of the canonical histone modifications that mark active enhancers in animals is consistent with the absence in plants of the bi-directional, short-lived enhancer RNAs found in animals (Erhard et al, 2015; Hetzel et al, 2016; Thieffry et al, 2020; Mcdonald et al, 2023; Silver et al, 2023). Thus, plants appear to use different mechanisms than animals for maintaining enhancer activity.…”

Section: Introductionsupporting

confidence: 75%

Cooperativity and additivity in plant enhancers

Jores,

Tonnies,

Mueth

et al. 2023

Preprint

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Enhancers arecis-regulatory elements that shape gene expression in response to numerous developmental and environmental cues. In animals, several models have been proposed to explain how enhancers integrate the activity of multiple transcription factors. However, it remains largely unknown how plant enhancers integrate transcription factor activity. Here, we use Plant STARR-seq to characterize three light-responsive plant enhancers—AB80,Cab-1, andrbcS-E9—derived from genes active in photosynthesis. Saturation mutagenesis reveals mutations, many of which cluster in short regions, that strongly reduce enhancer activity in the light, in the dark or in both conditions. When tested in the light, these mutation-sensitive regions do not function on their own; rather, cooperative interactions with other such regions are required for full activity. Epistatic interactions occur between mutations in adjacent mutation-sensitive regions, and the spacing and order of mutation-sensitive regions in synthetic enhancers affects enhancer activity. In contrast, when tested in the dark, mutation-sensitive regions act independently and additively in conferring enhancer activity. Taken together, this work demonstrates that plant enhancers show evidence for both cooperative and additive interactions among their functional elements. This knowledge can be harnessed to design strong, condition-specific synthetic enhancers.

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“…The study of cis-regulatory regions in plants have revealed similar molecular signatures 18 , although H3K4me1 is found in gene bodies rather than distal enhancers 9,19,20 , and the presence of enhancer RNAs is disputed 21 . The catalog of distal elements in maize has been greatly improved by recent efforts to resolve cell-type specific accessible regions with single-cell ATAC-seq experiments 9,19,22 .…”

Section: Introductionmentioning

confidence: 99%

MaizeCODE reveals bi-directionally expressed enhancers that harbor molecular signatures of maize domestication

Cahn,

Regulski,

Lynn

et al. 2024

Preprint

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Modern maize was domesticated fromTeosinte parviglumis, with subsequent introgressions fromTeosinte mexicana, yielding increased kernel row number, loss of the hard fruit case and dissociation from the cob upon maturity, as well as fewer tillers. Molecular approaches have identified several transcription factors involved in the development of these traits, yet revealed that a complex regulatory network is at play. MaizeCODE deploys ENCODE strategies to catalog regulatory regions in the maize genome, generating histone modification and transcription factor ChIP-seq in parallel with transcriptomics datasets in 5 tissues of 3 inbred lines which span the phenotypic diversity of maize, as well as the teosinte inbred TIL11. Integrated analysis of these datasets resulted in the identification of a comprehensive set of regulatory regions in each inbred, and notably of distal enhancers which were differentiated from gene bodies by their lack of H3K4me1. Many of these distal enhancers expressed non- coding enhancer RNAs bi-directionally, reminiscent of “super enhancers” in animal genomes. We show that pollen grains are the most differentiated tissue at the transcriptomic level, and share features with endosperm that may be related to McClintock’s chromosome breakage- fusion-bridge cycle. Conversely, ears have the least conservation between maize and teosinte, both in gene expression and within regulatory regions, reflecting conspicuous morphological differences selected during domestication. The identification of molecular signatures of domestication in transcriptional regulatory regions provides a framework for directed breeding strategies in maize.

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Enhancers associated with unstable RNAs are rare in plants

Cited by 3 publications

References 78 publications

Plant enhancers exhibit both cooperative and additive interactions among their functional elements

Plant enhancers exhibit both cooperative and additive interactions among their functional elements

Cooperativity and additivity in plant enhancers

MaizeCODE reveals bi-directionally expressed enhancers that harbor molecular signatures of maize domestication

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