A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici

Abstract

Background:The 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. Results: Here, 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 transcriptomeassisted 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.Conclusions: Taken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.

Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen

“…The dim2 DNA methyltransferase gene is functional in several Z. tritici isolates Based on our identification of a non-truncated dim2 gene in an Iranian Z. tritici isolate, Zt10, we set out to investigate its recent evolution in the Zymoseptoria species complex in a much larger collection of genome sequences than previously [25] available. We used BLAST to search for the sequence of dim2 in 22 high-quality assemblies obtained by SMRT sequencing of Z. tritici (Fig 1) [33][34][35][36], as well as 17 genomes of Z. ardabiliae, and nine genomes of Z. brevis (S1 Table), both closely related sister species of Z. tritici and considered to be endemic to Iran. We detected a single dim2 homolog in each of the Z. ardabiliae and Z. brevis genomes but found multiple mutated and non-functional copies of dim2 in 17 out of 22 Z. tritici genomes (Fig 1).…”

“…Non-functional copies contained numerous mutations including pre-mature stop codons. [33,37], and one is from Tunisia (TN09, collected from durum wheat) [33]. We further tested whether presence of a non-mutated dim2 allele is commonly found among Iranian isolates.…”

“…All analyzed genomes and isolates used in this study are listed in Table S1 and originate from the following studies [32,33,[77][78][79][80][81][34][35][36][37]48,49,71,76]. We identified homologs of dim2 using the predicted 'deRIPed' protein sequence of Z. tritici IPO323 [25] as a template.…”

Fungicide Sensitivity Shifting of Zymoseptoria tritici in the Finnish-Baltic Region and a Novel Insertion in the MFS1 Promoter

“…Manual and in silico analysis of the promoter insert sequence, following the guidelines proposed by Wicker et al (2007) for TE analysis, allowed us to detect the target site duplication (TSD) 5 TA/CTCGTG 3 , inversed at the opposite end, and a rather long terminal inverted repeat of 62 bp (with four mismatches). In recent work, Badet et al (2020) have annotated TEs in the Z. tritici pangenome. Sequences highly similar to the MFS1 promoter insert of strain 18-Zt-EE-06-03 were annotated as DTT_Birute transposon family of the Tc1-Mariner superfamily, class II DNA transposons (Oggenfuss and Croll, personal communication) according to the nomenclature proposed by Wicker et al (2007).…”

Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

“…We also identify accessory signatures in core chromosomes, including the previously described right arm of chromosome 7 [6]. Although this region has not been reported to share the same extent of presenceabsence polymorphism as the accessory chromosomes, a considerably smaller chromosome 7 was reported in a single Z. tritici isolate originating from Yemen [33]. Here we show that the region homologous to chromosome 7 in the other Zymoseptoria species also exhibits accessory compartment hallmarks.…”