A. Foliar lesions induced by Zymoseptoria tritici on wheat leaves. B. Zymoseptoria tritici pseudothecia and ascospores (sexual reproduction). C. Zymoseptoria tritici pycnidiospores (asexual reproduction). D. RAxML phylogram constructed from ITS, LSU, tef1, and rpb2 sequences of all accepted species of Zymoseptoria (Chen et al. Studies in Mycology 101: 417–564, 2022). Photo Credits: Janine Haueisen - Environmental Genomics, Max Planck Institute for Evolutionary Biology (A); Frederic Suffert - Université Paris-Saclay, INRAE. (B and C)

Zymoseptoria tritici (syn. Mycosphaerella graminicola) is a haploid, heterothallic Ascomycotina (Capnodiales; Dothideomycetes). The Zymoseptoria genus gathers seven additional species. Z. pseudotritici, Z. ardabiliae, Z. brevis, Z. verkleyi and Z. crescenta were isolated from wild grasses in Iran. Z. passerinii and Z. halophila were isolated from barley worldwide. The closest genus to Zymoseptoria is Ramularia that includes the barley pathogen Ramularia collo-cygni.

Z. tritici is a major fungal pathogen of wheat, responsible for the Septoria tritici blotch (STB) foliar disease. The infection process of Z. tritici is bi-phasic. Z. tritici acts like an endophyte during its asymptomatic phase and behaves as a destructive pathogen during its necrotrophic phase. Both sexual and asexual reproduction are observed in infected wheat fields. The disease is difficult to control, as the emergence of fungicide-resistant isolates has reduced the efficacy of many fungicides. Likewise, all resistant wheat cultivars carrying major resistance genes (Stb genes) have been defeated by the emergence of virulent isolates. Integrated disease management is required to control this disease.

Z. tritici is a major experimental model to study plant−fungal interactions, their evolutionary dynamics as well as their molecular basis. Z. tritici can be propagated in liquid and on solid media. The fungus is dimorphic as it displays both filamentous (hyphae) and yeast-like growth (blastospores) depending on culture conditions (media, temperature, host plant). It also differentiates chlamydospores, pycnidia, and pycinidiospores (asexual reproduction) in vitro. Z. tritici has a bipolar, heterothallic sexual reproduction, and experimental crosses can be performed on wheat leaves infected with isolates of opposite mating types.

IPO323 Z. tritici genome sequence was released in 2011 (Goodwin et al., 2011). This 39.7 Mb sequence comprised a total of 21 chromosomes which have been completely assembled from telomere to telomere. Centromeres of each chromosome of IPO323 have been mapped using ChIP-seq. The IPO323 Z. tritici genome is composed of 13 core chromosomes (CCs: 1.2−6.1 Mb) conserved across isolates, and 8 accessory chromosomes (ACs: 0.4−0.8 Mb), varying in number and size among Z. tritici isolates. Additional genomes of Z. tritici isolates from different geographic origins varied in size from 37.1 to 41.7 Mb, with 13 CCs and 4−8 ACs. Their gene repertoires highlighted a pangenome of 15,451 genes, among which 60 % were conserved across all isolates (core), and 40 % were accessory. IPO323 genome TE content was estimated between 17% and 20%. The most abundant TEs in Z. tritici were LTR-Gypsy and LTR-Copia Class I retroelements (70%), followed by Class II DNA transposons (22%). The distribution of TEs in the genome was not random, as AC chromosomes display a 2-fold higher content than CCs. A significant proportion of Z. tritici TEs (70%) was expressed, and specific TE families showed a high level of expression during infection or under specific stress conditions.

Four previous IPO323 annotations identified 10,933 to 13,260 gene models, but only one-third of these coding sequences were found to have identical structures. Novel data and annotation tools (IPO323 Iso-Seq and RNA-Seq transcripts, fungal protein sequences) were used to select the best structure among gene models from different annotation pipelines using InGenAnnot (Lapalu et al., 2023). 13,414 re-annotated gene models were predicted, including 671 new genes. This process improved 15-40 % of the previous gene models depending on the pipeline. 5’ and 3’UTRs were also predicted for 73% of the gene models.