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

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

doi:10.1371/journal.pgen.1007467

David J Winter, Carolyn A Young + Show 8 more

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https://doi.org/10.1371/journal.pgen.1007467

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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.

Highlights

The three-dimensional organisation of chromatin within the nucleus is increasingly seen as a key contributor to the regulation of gene expression [1,2,3]
Using chromosome conformation to investigate the three-dimensional structure of the genome, we show that these repeat-rich blocks mediate genome folding within the nucleus, and this genome structure in turn contributes to the modulation of gene expression, notably for those genes that are strongly differentially expressed in planta
Interspersed AT-rich sequences are a feature of some fungal genomes, the E. festucae sequence is remarkable for the proportion of its genome contained in these regions and the preponderance of long AT-rich blocks

Summary

Introduction

The three-dimensional organisation of chromatin within the nucleus is increasingly seen as a key contributor to the regulation of gene expression [1,2,3]. Nuclear organisation is increasingly understood to be important, our present knowledge of how this organisation is maintained and its contribution to gene expression are limited to a small number of model species We extend such investigations to a non-model filamentous fungus. Epichloë species can have profound effects on their hosts, including resistance to herbivory by mammals [18] and insects [19,20], resistance to nematodes [21] and non-Epichloë competitor fungi [22], and increased drought tolerance [23,24,25] This intimate symbiotic relationship, and the powerful techniques available to interrogate the Epichloë-grass interaction [15,26,27], make this the most well-developed system in which to study an above-ground interaction between a fungus and a plant [16,28]

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