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PLoS Genet. 2018 Oct 24;14(10):e1007467. doi: 10.1371/journal.pgen.1007467. eCollection 2018 Oct.

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

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Statistics and Bioinformatics Group, Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand.
The Bio-Protection Research Centre, Massey University, Palmerston North, New Zealand.
School of Biological Sciences, University of Auckland, Auckland, New Zealand.
Noble Research Institute, LLC, Ardmore, Oklahoma, United States of America.
Phase Genomics Inc, Seattle, Washington, United States of America.
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, United States of America.
Genetics Group, Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand.


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.

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