Repeat Elements Organise 3D Genome Structure and Mediate Transcription in the Filamentous Fungus Epichloë festucae

Authors

David J. Winter, Massey University, New Zealand
Austen R. D. Ganley, Universityof Auckland, New Zealand
Carolyn A. Young, Noble Research Institute, LLC
Ivan Liachko, Phase Genomics Inc.
Christopher L. Schardl, University of KentuckyFollow
Pierre-Yves Dupont, Massey University, New Zealand
Daniel Berry, Massey University, New Zealand
Arvina Ram, Massey University, New Zealand
Barry Scott, Massey University, New Zealand
Murray P. Cox, Massey University, New Zealand

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.

Document Type

Article

Publication Date

10-24-2018

Notes/Citation Information

Published in PLOS Genetics, v. 14, no. 10, e1007467, p. 1-29.

© 2018 Winter et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Digital Object Identifier (DOI)

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

Funding Information

his 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.

Related Content

A software repository providing the scripts used to produce the computational results described above is available at https://github.com/dwinter/fl1_genome_scripts. Data underlying these analyses have been deposited at NCBI under two Bioprojects. Project PRJNA431450 contains genomic data and project PRJNA447872 contains RNAseq data.

S1 Fig. Repeat classes are not uniformly distributed among AT- and gene-rich regions. https://doi.org/10.1371/journal.pgen.1007467.s001 (TIF)

S2 Fig. There are few full-length copies of longer repeats. https://doi.org/10.1371/journal.pgen.1007467.s002 (TIF)

S3 Fig. Transcontacts are dominated by AT-AT and centromere-centromere interactions. https://doi.org/10.1371/journal.pgen.1007467.s003 (TIF)

S4 Fig. Within chromosome contacts are dominated by interactions between regions of similar GC-content. https://doi.org/10.1371/journal.pgen.1007467.s004 (TIF)

S5 Fig. ApG dinucleotides are most likely to experience 6mA modification. https://doi.org/10.1371/journal.pgen.1007467.s005 (TIF)

S1 Table. Summary data for repeat annotation. https://doi.org/10.1371/journal.pgen.1007467.s006 (CSV)

S2 Table. Genes falling in co-regulated TADs. https://doi.org/10.1371/journal.pgen.1007467.s007 (CSV)

S3 Table. Summary statistics for PacBio sequencing library. https://doi.org/10.1371/journal.pgen.1007467.s008 (CSV)

S4 Table. Summary statistics for genome assembly. https://doi.org/10.1371/journal.pgen.1007467.s009 (CSV)

S5 Table. Summary statistics for previously available E. festucae Fl1 assemblies. https://doi.org/10.1371/journal.pgen.1007467.s010 (CSV)

Repository Citation

Winter, David J.; Ganley, Austen R. D.; Young, Carolyn A.; Liachko, Ivan; Schardl, Christopher L.; Dupont, Pierre-Yves; Berry, Daniel; Ram, Arvina; Scott, Barry; and Cox, Murray P., "Repeat Elements Organise 3D Genome Structure and Mediate Transcription in the Filamentous Fungus Epichloë festucae" (2018). Plant Pathology Faculty Publications. 86.
https://uknowledge.uky.edu/plantpath_facpub/86