Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

Abstract

Background: Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure. Results: Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts. Conclusion: Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.

Genome-wide mapping of histone modifications during axenic growth in two species of Leptosphaeria maculans showing contrasting genomic organization

“…The distinct genome organization shown by Lmb and Lml thus provides us with a model of choice for comparing epigenomic organization in two closely related phytopathogenic fungi, to determine the genomic location of pathogenicity/effector genes in relation to the chromatin landscape and the influence of chromatin structure on gene expression. Comparative epigenomic analyses, at the intra-or inter-species levels, are very sparse and this remains an underexplored field of study, at least in fungi (Zhang et al 2018;Feurtey et al 2019). We present here the first comparative epigenomic analysis of both euchromatin and heterochromatin marks in two closely related phytopathogenic fungi.…”

Natural variation in Avr3D1 from Zymoseptoria sp. contributes to quantitative gene‐for‐gene resistance and to host specificity

“…The genomes of these three Zymoseptoria species are highly similar, with 6% divergence at the nucleotide level between Z. tritici and Z. pseudotritici and 10% between Z. tritici and Z. ardabiliae (Stukenbrock et al ., 2011). Consequently, several effector genes of Z. tritici are also found in the genomes of Z. pseudotritici and Z. ardabiliae (Stukenbrock et al ., 2011; Feurtey et al ., 2019). Although effectors have been suggested to be involved in adaptation of Z. tritici to wheat, their role in host specialization remains unclear (Stukenbrock et al ., 2011; Poppe et al ., 2015; Lorrain et al ., 2021).…”

A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen

“…The fungal wheat pathogen Zymoseptoria tritici is one of the most important pathogens on crops causing high yield losses (Torriani et al, 2015). The genome is completely assembled and shows size variation between individuals sampled across the global distribution range (Feurtey et al, 2020;Badet et al, 2020) (Goodwin et al, 2011). The TE content of the genome shows a striking variation of 17-24% variation among individuals (Badet et al, 2020).…”