Intraspecific variation of transposable elements reveals differences in the evolutionary history of fungal phytopathogen pathotypes

Abstract

Fungal plant pathogens pose a significant threat to biodiversity and food security worldwide. This threat is aggravated by their rapidly evolving genomes that adapt to evade host plant defenses, reducing the efficacy of deployed resistant crops.Magnaporthe oryzaeinfects rice, wheat, and many other grasses, resulting in significant crop losses each year. Transposable elements (TEs) are hypothesized to be involved in the evolution and rapid adaptation ofM. oryzae. However, there is still much to understand about how these elements behave in differentM. oryzaehost-specific lineages. In this study, we completed the annotation and phylogenetic classification of TEs in five lineages ofM. oryzae. We identified differences in TE content between these lineages, and showed that recent lineage-specific expansions of certain TEs have contributed to greater TE content in rice-infecting andSetaria-infecting lineages. We reconstructed the histories of LTR-retrotransposon expansions and found them to have experienced complex dynamics, where some were caused by the proliferation of one element, while others consisted of multiple elements from an older population of TEs that proliferated in parallel. Additionally, we found evidence suggesting the recent transfer of a DNA transposon between rice and wheatM. oryzaelineages, and a region showing evidence of recombination between those lineages, which could have facilitated such a transfer. These results point towards key differences in TE dynamics, evolutionary history, and adaptive potential between the rice-and-Setaria-infecting and the wheat-Lolium-and-Eleusine-infecting lineage groups.

Distinct genomic contexts predict gene presence-absence variation in different pathotypes of a fungal plant pathogen

“…A previous report has shown that MoO has a much greater TE content than MoT [20]. Therefore, given this result and the greatly increased number of PAV orthogroups in MoT compared to MoO we observed (Fig.…”

“…The two M. oryzae pathotypes share some major differences in their TE content [20] and very different life histories, with MoO originating 9,800 thousand years ago [17] and propagating mostly clonally since then, while MoT is thought to have emerged approximately 60 years ago from a multi-hybrid swarm of many different M. oryzae pathotypes [12,16]. We propose that the differences in PAV across the two pathotypes may reflect these life histories, with MoO exhibiting more of a stable equilibrium and much slower paced evolution, where PAV events happen in specifically defined compartments of the genome, while MoT is rapidly losing and gaining genes, even in areas of the genome where most of the conserved genes in MoO are located.…”

“…TE annotation was performed using RepeatMasker [46] version 4.1.1 and a reference TE library for all pathotypes of M. oryzae generated by Nakamoto et al . [20]. The parameters -cutoff 250, -nolow, -no_is, and -norna were used for the RepeatMasker command.…”

Pyricularia oryzae: Lab star and field scourge

“…Repeated genetic elements contribute to genome plasticity in P. oryzae . The content in transposable elements and repeat sequences in P. oryzae genomes varies between 5% and 11%, which is moderate for phytopathogenic ascomycetes (Chiapello et al., 2015; Dean et al., 2005; Nakamoto et al., 2023). Genes that show presence/absence polymorphism between lineages are frequently associated with transposable elements, suggesting that transposons are implicated in their acquisition and/or loss (Yoshida et al., 2016).…”