Identifying synergistic high-order 3D chromatin conformations from genome-scale nanopore concatemer sequencing

Deshpande, Aditya; Ulahannan, Netha; Pendleton, Matthew; Dai, Xiaofeng; Ly, Lynn; Behr, Julie M.; Schwenk, Stefan; Liao, Will; Augello, Michael A.; Tyer, Carly; Rughani, Priyesh; Kudman, Sarah; Tian, Huasong; Otis, Hannah G.; Adney, Emily M.; Wilkes, David; Mosquera, Juan Miguel; Barbieri, Christopher E.; Melnick, Ari; Stoddart, David; Turner, Daniel J.; Juul, Sissel; Harrington, Eoghan; Imieliński, Marcin

doi:10.1038/s41587-022-01289-z

Cited by 70 publications

(89 citation statements)

References 72 publications

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“…To further characterize rice dREG distal peaks and identify potential functional roles in the rice genome, we examined long-range chromosomal contact interaction between genes and candidate CREs using the Pore-C sequencing method [72]. Pore-C couples chromatin conformation capture with long-read nanopore sequencing to detect genome-wide multi-way chromatin contacts.…”

Section: Resultsmentioning

confidence: 99%

“…Pore-C couples chromatin conformation capture with long-read nanopore sequencing to detect genome-wide multi-way chromatin contacts. It has been shown to be highly effective at sequencing through repeat regions of the genome and is able to detect increased contact intensity with less sequencing reads than conventional Hi-C sequencing [72]. Using Pore-C sequencing on rice leaves, we generated 104 million concatamer reads that correspond to 290 million contacts across the rice genome (Additional file 2: Table S2).…”

Section: Resultsmentioning

confidence: 99%

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Nascent transcription and the associatedcis-regulatory landscape in rice

Choi

Platts

Johary

et al. 2022

Preprint

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Background Plant genomes encode transcripts that require spatio-temporal regulation for proper cellular function, and a large fraction of the regulators can be found in intergenic regions. In animals, distal intergenic regions described as enhancer regions are actively transcribed as enhancer RNAs (eRNAs); the existence of eRNAs in plants has only been fairly recently documented. In this study, we evaluated with high sensitivity the synthesis of eRNAs that arise at genomic elements both distal and proximal to genes by combining PRO-seq with chromatin accessibility, histone modification, and methylation profiles in rice. Results We found that regions defined as transcribed intergenic regions are widespread in the rice genome, and many likely harbor transcribed regulatory elements. In addition to displaying evidence of selective constraint, the presence of these transcribed regulatory elements are correlated with an increase in nearby gene expression. We further identified molecular interactions between genic regions and intergenic transcribed regulatory elements using 3D chromosomal contact data, and found that these interactions were both associated with eQTLs as well as promoting transcription. We also compared the profile of accessible chromatin regions to our identified transcribed regulatory elements, and found less overlap than expected. Finally, we also observed that transcribed intergenic regions that overlapped partially or entirely with repetitive elements had a propensity to be enriched for cytosine methylation, and were likely involved in TE silencing rather than promoting gene transcription. Conclusion The characterization of eRNAs in the rice genome reveals that many share features of enhancers and are associated with transcription regulation, which could make them compelling candidate enhancer elements.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Nascent transcription and the associatedcis-regulatory landscape in rice

Choi

Platts

Johary

et al. 2022

Preprint

View full text Add to dashboard Cite

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“…Limited by experimental principles, Hi‐C does not perform well for exploring multiple interactions (Lieberman‐Aiden et al., 2009). However, Pore‐C can complement this shortcoming by intracellular cross‐linking, in situ digestion (DpnII), in situ proximity ligation, reverse cross‐linking and Nanopore long‐read sequencing (Figure 1a; Deshpande et al., 2022). To construct a fine 3D genome map of cotton, we produced an ultra‐high‐resolution (3 Kb) Hi‐C library (233 Gb) and a Pore‐C library (113 Gb) with appropriate resolution (20 Kb) using leaves of G. hirsutum (Figure 1b, Tables S1 and S2).…”

Section: Figurementioning

confidence: 99%

Multi‐omics mapping of chromatin interaction resolves the fine hierarchy of 3D genome in allotetraploid cotton

Huang

Tian

Pei

et al. 2022

Plant Biotechnology Journal

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“…g, Comparison of the costs per million virtual pairwise contacts between HiPore-C (blue for GM12878 and orange for K562), Pore-C (gray dotted line) 57 , and Hi-C (red line).…”

Section: Interchromosomal Interaction Hubsmentioning

confidence: 99%

“…Theoretically, multiway interactions between fragments in a single read can be used to identify synergistic interactions directly and to acquire single-allele topology in a cell population. In fact, a few methods that generate multiway chromatin contacts have been developed, including genome architecture mapping (GAM) 52 , ChIA-drop 53 , split-pool recognition of interactions by tag extension (SPRITE) 6,54 , Tri-C 55 , multicontact 4C 43 , concatemer ligation assay (COLA) 56 , and Pore-C 57 . Among these methods, Pore-C stands out because it can capture global high-order multiway contacts, is technically simple, and captures DNA methylation simultaneously in a cell population.…”

Section: Introductionmentioning

confidence: 99%

High-throughput Pore-C reveals the single-allele topology polymorphism and cell type specificity of 3D genome folding

Xiao

Zhong

Niu

et al. 2022

Preprint

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Canonical three-dimensional (3D) genome structures represent the ensemble average of pairwise chromatin interactions but not the single-allele topologies in populations of cells. Recently developed Pore-C can capture multiway chromatin contacts that reflect regional topologies of single chromosomes. By carrying out high-throughput Pore-C, we reveal extensive but regionally restricted clusters of single-allele topologies that aggregate into canonical 3D genome structures in two human cell types. We show that fragments in multicontact reads generally coexist in the same TAD, while a concurrent significant proportion of multicontact reads span multiple compartments of the same chromatin type over megabase distances. Synergistic chromatin looping between multiple sites in multicontact reads is extremely rare compared to pairwise interactions. Interestingly, the single-allele topology clusters are cell type-specific even inside highly conserved TADs in different types of cells. In summary, HiPore-C enables global characterization of single-allele topologies at an unprecedented depth to reveal elusive genome folding principles.

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Identifying synergistic high-order 3D chromatin conformations from genome-scale nanopore concatemer sequencing

Cited by 70 publications

References 72 publications

Nascent transcription and the associatedcis-regulatory landscape in rice

Nascent transcription and the associatedcis-regulatory landscape in rice

Multi‐omics mapping of chromatin interaction resolves the fine hierarchy of 3D genome in allotetraploid cotton

High-throughput Pore-C reveals the single-allele topology polymorphism and cell type specificity of 3D genome folding

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