Abstract

BackgroundThe gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures.ResultsHere, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only ~ 60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable element content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species.ConclusionsTaken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.

Highlights

  • The gene content of a species largely governs its ecological interactions and adaptive potential

  • Major chromosomal rearrangements segregating within the species We constructed a global pangenome of Z. tritici based on 19 isolates sampled from six continents and 13 different countries (Fig. 1a, b)

  • The isolates included the previously described reference isolate IPO323 sampled in the Netherlands and four isolates that were isolated from two nearby fields in Switzerland [27, 28, 40]

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Summary

Introduction

The gene content of a species largely governs its ecological interactions and adaptive potential. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content It remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. Large pangenomes can challenge association studies aiming to identify the genetic basis of phenotypic traits because mapping is often performed against a single reference genome, making potentially relevant genetic variation inaccessible [9, 10]. Despite their importance for unraveling the genetic basis of adaptive evolution, only a very limited number of eukaryotic species have well established pangenomes

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