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Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation.

ABSTRACT: Insight into high-resolution three-dimensional genome organization and its effect on transcription remains largely elusive in plants. Here, using a long-read ChIA-PET approach, we map H3K4me3- and RNA polymerase II (RNAPII)-associated promoter-promoter interactions and H3K9me2-marked heterochromatin interactions at nucleotide/gene resolution in rice. The chromatin architecture is separated into different independent spatial interacting modules with distinct transcriptional potential and covers approximately 82% of the genome. Compared to inactive modules, active modules possess the majority of active loop genes with higher density and contribute to most of the transcriptional activity in rice. In addition, promoter-promoter interacting genes tend to be transcribed cooperatively. In contrast, the heterochromatin-mediated loops form relative stable structure domains in chromatin configuration. Furthermore, we examine the impact of genetic variation on chromatin interactions and transcription and identify a spatial correlation between the genetic regulation of eQTLs and e-traits. Thus, our results reveal hierarchical and modular 3D genome architecture for transcriptional regulation in rice.

SUBMITTER: Zhao L

PROVIDER: S-EPMC6692402 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation.

Zhao Lun L Wang Shuangqi S Cao Zhilin Z Ouyang Weizhi W Zhang Qing Q Xie Liang L Zheng Ruiqin R Guo Minrong M Ma Meng M Hu Zhe Z Sung Wing-Kin WK Zhang Qifa Q Li Guoliang G Li Xingwang X

Nature communications 20190813 1

Insight into high-resolution three-dimensional genome organization and its effect on transcription remains largely elusive in plants. Here, using a long-read ChIA-PET approach, we map H3K4me3- and RNA polymerase II (RNAPII)-associated promoter-promoter interactions and H3K9me2-marked heterochromatin interactions at nucleotide/gene resolution in rice. The chromatin architecture is separated into different independent spatial interacting modules with distinct transcriptional potential and covers a ...[more]

PMID: 31409785

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Project description:Rice has the natural morphological adaptation to germinate and elongate its coleoptile under submerged flooding conditions. The phenotypic deviation associated with the tolerance to submergence at the germination stage could be due to natural variation. However, the molecular basis of this variation is still largely unknown. A comprehensive understanding of gene regulation of different genotypes that have diverse rates of coleoptile elongation can provide significant insights into improved rice varieties. To do so, publicly available transcriptome data of five rice genotypes, which have different lengths of coleoptile elongation under submergence tolerance, were analyzed. The aim was to identify the correlation between promoter architecture, associated with transcriptional and hormonal regulation, in diverse genotype groups of rice that have different rates of coleoptile elongation. This was achieved by identifying the putative cis-elements present in the promoter sequences of genes upregulated in each group of genotypes (tolerant, highly tolerant, and extremely tolerant genotypes). Promoter analysis identified transcription factors (TFs) that are common and unique to each group of genotypes. The candidate TFs that are common in all genotypes are MYB, bZIP, AP2/ERF, ARF, WRKY, ZnF, MADS-box, NAC, AS2, DOF, E2F, ARR-B, and HSF. However, the highly tolerant genotypes interestingly possess binding sites associated with HY5 (bZIP), GBF3, GBF4 and GBF5 (bZIP), DPBF-3 (bZIP), ABF2, ABI5, bHLH, and BES/BZR, in addition to the common TFs. Besides, the extremely tolerant genotypes possess binding sites associated with bHLH TFs such as BEE2, BIM1, BIM3, BM8 and BAM8, and ABF1, in addition to the TFs identified in the tolerant and highly tolerant genotypes. The transcriptional regulation of these TFs could be linked to phenotypic variation in coleoptile elongation in response to submergence tolerance. Moreover, the results indicate a cross-talk between the key TFs and phytohormones such as gibberellic acid, abscisic acid, ethylene, auxin, jasmonic acid, and brassinosteroids, for an altered transcriptional regulation leading to differences in germination and coleoptile elongation under submergence. The information derived from the current in silico analysis can potentially assist in developing new rice breeding targets for direct seeding.

Project description:BackgroundHistone chaperones modulate chromatin architecture and hence play a pivotal role in epigenetic regulation of gene expression. In contrast to their animal and yeast counterparts, not much is known about plant histone chaperones. To gain insights into their functions in plants, we sought to identify histone chaperones from two model plant species and investigated their phylogeny, domain architecture and transcriptional profiles to establish correlation between their expression patterns and potential role in stress physiology and plant development.ResultsThrough comprehensive whole genome analyses of Arabidopsis and rice, we identified twenty-two and twenty-five genes encoding histone chaperones in these plants, respectively. These could be classified into seven different families, namely NAP, CAF1, SPT6, ASF1, HIRA, NASP, and FACT. Phylogenetic analyses of histone chaperones from diverse organisms including representative species from each of the major plant groups, yeast and human indicated functional divergence in NAP and CAF1C in plants. For the largest histone chaperone family, NAP, phylogenetic reconstruction suggested the presence of two distinct groups in plants, possibly with differing histone preferences. Further, to comment upon their physiological roles in plants, we analyzed their expression at different developmental stages, across various plant tissues, and under biotic and abiotic stress conditions using pre-existing microarray and qRT-PCR. We found tight transcriptional regulation of some histone chaperone genes during development in both Arabidopsis and rice, suggesting that they may play a role in genetic reprogramming associated with the developmental process. Besides, we found significant differential expression of a few histone chaperones under various biotic and abiotic stresses pointing towards their potential function in stress response.ConclusionsTaken together, our findings shed light onto the possible evolutionary trajectory of plant histone chaperones and present novel prospects about their physiological roles. Considering that the developmental process and stress response require altered expression of a large array of genes, our results suggest that some plant histone chaperones may serve a regulatory role by controlling the expression of genes associated with these vital processes, possibly via modulating chromatin dynamics at the corresponding genetic loci.

Dataset Information

Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation.

Publications

Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation.

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