Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

Abstract

The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage: Septoria tritici) causes septoria tritici blotch, a disease that greatly reduces the yield and quality of wheat. This disease is economically important in most wheat-growing areas worldwide and threatens global food production. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity, including mechanisms of infection and of resistance in the host. Unlike most other plant pathogens, M. graminicola has a long latent period during which it evades host defenses. Although this type of stealth pathogenicity occurs commonly in Mycosphaerella and other Dothideomycetes, the largest class of plant-pathogenic fungi, its genetic basis is not known. To address this problem, the genome of M. graminicola was sequenced completely. The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable. This eight-chromosome dispensome is dynamic in field and progeny isolates, is different from the core genome in gene and repeat content, and appears to have originated by ancient horizontal transfer from an unknown donor. Synteny plots of the M. graminicola chromosomes versus those of the only other sequenced Dothideomycete, Stagonospora nodorum, revealed conservation of gene content but not order or orientation, suggesting a high rate of intra-chromosomal rearrangement in one or both species. This observed “mesosynteny” is very different from synteny seen between other organisms. A surprising feature of the M. graminicola genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to pathogens. The stealth pathogenesis of M. graminicola probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from endophytic ancestors.

Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen

“…Various mechanisms have been described that facilitate rapid development of novel effector genes in pathogenic microbes, including diversity at genomic locations enriched for transposons, mutation, and recombination in subtelomeric regions (McDonagh et al 2008;Chuma et al 2011), coregulated gene clusters (Pallmer and Keller 2010;Schirawski et al 2010), small dispensable chromosomes (Coleman et al 2009;Ma et al 2010;Stukenbrock et al 2010;Goodwin et al 2011;Raffaele and Kamoun 2012), gene sparse regions (Raffaele et al 2010), ATrich isochore-like regions (van der Wouw et al 2010; Rouxel et al 2011), genome hybridization , and horizontal gene transfer (Friesen et al 2006;de Jonge et al 2012;Gardiner et al 2012). However, most of these mechanisms have been described in species that can reproduce sexually, and of which the genomes were shaped by repeat-driven expansion (Raffaele and Kamoun 2012).…”

“…This is significantly less when compared with the genomes of other filamentous pathogens, such as the fungi Magnaporthe oryzae (10%), Z. tritici (17%), Fusarium oxysporum (28%), Cladosporium fulvum Cold Spring Harbor Laboratory Press on April 27, 2019 -Published by genome.cshlp.org Downloaded from (47%), Blumeria graminis (64%), and the oomycetes Hyaloperonospora arabidopsidis (42%) and Phytophthora infestans (74%) (Dean et al 2005;Haas et al 2009;Baxter et al 2010;Ma et al 2010;Spanu et al 2010;Goodwin et al 2011;de Wit et al 2012). Comparative analyses between highly similar V. dahliae strains revealed numerous intra-and interchromosomal rearrangements and extensive karyotype variation.…”

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…We used complete genome assemblies of IPO323, ST99CH_3D1 (3D1), ST99CH_3D7 (3D7), ST99CH_1E4 (1E4) and ST99CH_1A5 (1A5) previously described by Goodwin et al . (2011) and Plissonneau et al . (2016, 2018).…”

A new class of fatty acid allene oxide formed by the DOX-P450 fusion proteins of human and plant pathogenic fungi, C. immitis and Z. tritici

“…The two allene oxides, 8R(9)-and 8S(9)-epoxy-9-octadecamonoenoic acids (EOMEs), are mainly hydrolyzed to -ketols by inversion of configuration at C-8 (solid arrows). wheat (22,23). Plants transform 13S-HPOTrE sequentially to allene oxides and to jasmonates, which act as growth and defense hormones (37,38).…”

“…Zymoseptoria tritici (teleomorph Mycosphaerella graminicola) causes the most important disease of wheat, septoria tritici blotch (22,23). Little is known about the DOX-CYP enzymes of these important pathogens.…”