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Origin of RNA Polymerase II pause in eumetazoans: Insights from Hydra

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Abstract

Multicellular organisms have evolved sophisticated mechanisms for responding to various developmental, environmental and physical stimuli by regulating transcription. The correlation of distribution of RNA Polymerase II (RNA Pol II) with transcription is well established in higher metazoans, however genome-wide information about its distribution in early metazoans, such as Hydra, is virtually absent. To gain insights into RNA Pol II-mediated transcription and chromatin organization in Hydra, we performed chromatin immunoprecipitation (ChIP)-coupled high-throughput sequencing (ChIP-seq) for RNA Pol II and Histone H3. Strikingly, we found that Hydra RNA Pol II is uniformly distributed across the entire gene body, as opposed to its counterparts in bilaterians such as human and mouse. Furthermore, correlation with transcriptome data revealed that the levels of RNA Pol II correlate with the magnitude of gene expression. Strikingly, the characteristic peak of RNA Pol II pause typically observed in bilaterians at the transcription start sites (TSSs) was not observed in Hydra. The RNA Pol II traversing ratio in Hydra was found to be intermediate to yeast and bilaterians. The search for factors involved in RNA Pol II pause revealed that RNA Pol II pausing machinery was most likely acquired first in Cnidaria. However, only a small subset of genes exhibited the promoter proximal RNP Pol II pause. Interestingly, the nucleosome occupancy is highest over the subset of paused genes as compared to total Hydra genes, which is another indication of paused RNA Pol II at these genes. Thus, this study provides evidence for the molecular basis of RNA Pol II pause early during the evolution of multicellular organisms.

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Acknowledgements

The work was supported by the Centre of Excellence in Epigenetics program (BT/01/COE/09/07) of the Department of Biotechnology, Government of India to SG. KK acknowledges support from Genome Engineering Technologies programme (BT/PR25858/GET/119/169/2017) of the Department of Biotechnology, Government of India. PCR is supported by the Early Career Fellowship of the Wellcome Trust–DBT India Alliance (IA/E/16/1/503057).

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  1. Department of Biology, Indian Institute of Science Education and Research, Dr. Homi Bhabha Road, Pashan, Pune, 411 008, India

    Puli Chandramouli Reddy, Saurabh J Pradhan, Krishanpal Karmodiya & Sanjeev Galande

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  1. Puli Chandramouli Reddy
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  2. Saurabh J Pradhan
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  3. Krishanpal Karmodiya
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  4. Sanjeev Galande
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Correspondence to Krishanpal Karmodiya or Sanjeev Galande.

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This artice is part of the Topical Collection: Chromatin Biology and Epigenetics.

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Reddy, P.C., Pradhan, S.J., Karmodiya, K. et al. Origin of RNA Polymerase II pause in eumetazoans: Insights from Hydra. J Biosci 45, 8 (2020). https://doi.org/10.1007/s12038-019-9979-y

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