Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae

David J. Winter, Austen R.D. Ganley, Carolyn A. Young, Ivan Liachko, Christopher L. Schardl, Pierre Yves Dupont, Daniel Berry, Arvina Ram, Barry Scott, Murray P. Cox

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

Structural features of genomes, including the three-dimensional arrangement of DNA in the nucleus, are increasingly seen as key contributors to the regulation of gene expression. However, studies on how genome structure and nuclear organisation influence transcription have so far been limited to a handful of model species. This narrow focus limits our ability to draw general conclusions about the ways in which three-dimensional structures are encoded, and to integrate information from three-dimensional data to address a broader gamut of biological questions. Here, we generate a complete and gapless genome sequence for the filamentous fungus, Epichloë festucae. We use Hi-C data to examine the three-dimensional organisation of the genome, and RNA-seq data to investigate how Epichloë genome structure contributes to the suite of transcriptional changes needed to maintain symbiotic relationships with the grass host. Our results reveal a genome in which very repeat-rich blocks of DNA with discrete boundaries are interspersed by gene-rich sequences that are almost repeat-free. In contrast to other species reported to date, the three-dimensional structure of the genome is anchored by these repeat blocks, which act to isolate transcription in neighbouring gene-rich regions. Genes that are differentially expressed in planta are enriched near the boundaries of these repeat-rich blocks, suggesting that their three-dimensional orientation partly encodes and regulates the symbiotic relationship formed by this organism.

Original languageEnglish
Article numbere1007467
JournalPLoS Genetics
Volume14
Issue number10
DOIs
StatePublished - Oct 2018

Bibliographical note

Funding Information:
This research was supported by a grant from the Royal Society of New Zealand through a Rutherford Fellowship (RDF-10-MAU-001) to MPC, a Marsden grant (14-MAU-007) to MPC, ARDG and CAY; a Marsden grant (10-MAU-057) to BS; and by the Tertiary Education Commission via a Bio-Protection Research Centre grant to MPC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank colleagues for their helpful contributions: Justin O’Sullivan (University of Auckland); Romain Koszul (Institut Pasteur); Richard Johnson (AgResearch); Matthew Campbell (currently Hokkaido University); Yonathan Lukito and Tetsuya Chujo (Massey University).

Publisher Copyright:
© 2018 Winter et al. http://creativecommons.org/licenses/by/4.0/.

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Fingerprint

Dive into the research topics of 'Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae'. Together they form a unique fingerprint.

Cite this