Morphological changes in response to environmental stresses in the fungal plant pathogen Zymoseptoria tritici

Francisco, C. L.; Ma, Xin; Zwyssig, Maria Manuela; McDonald, Bruce A.; Palma‐Guerrero, Javier

doi:10.1038/s41598-019-45994-3

Cited by 94 publications

(127 citation statements)

References 86 publications

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“…Plant pathogens typically experience nutrient limitations while growing on leaves and the perception of a nutrient-limited environment may act as a stimulus to induce cell fusion in foliar plant pathogens. Both germinating blastospores or pycnidiospores of Z. tritici undergo CAT and VHF in vitro and in planta , supporting our previous observation (Francisco et al, 2019). Thus, we demonstrated that vegetative cell fusions occur independently of the morphotype and it may have an important contribution to the lifestyle of Z. tritici during the plant-pathogen interaction.…”

Section: Discussionsupporting

confidence: 91%

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The role of vegetative cell fusions in the lifestyle of the wheat fungal pathogenZymoseptoria tritici

Francisco¹,

Zwyssig²,

Palma‐Guerrero³

2020

Preprint

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26The ability of fungal cells to undergo cell fusion allows them to maximize their overall 27 fitness. In this study, we characterized the role of the so gene orthologous in 28Zymoseptoria tritici and the biological contribution of vegetative cell fusions in the 29 lifestyle of this latent necrotrophic fungus. Firstly, we show that Z. tritici undergoes 30 self-fusion between distinct cellular structures and its mechanism is dependent on the 31 initial cell density. Next, the deletion of ZtSo resulted in the loss of cell-to-cell 32 communication affecting both hyphal and germlings fusion. We show that Z. tritici 33 mutants for MAP kinase-encoding ZtSlt2 (orthologous MAK-1) and ZtFus3 34 (orthologous MAK-2) genes also fail to undergo self-stimulation and self-fusion, 35demonstrating the functional conservation of this signaling mechanism across 36 species. Additionally, the DZtSo mutant was severely impaired in melanization, which 37 leads us to identify a trade-off between fungal growth and melanization. Though it has 38 been proposed that So is a scaffold protein for MAP kinase genes from the CWI 39 pathway, its deletion did not affect the cell wall integrity of the fungus. Finally, we 40 demonstrated that anastomose is dispensable for pathogenicity, but essential for the 41 fruiting body development and its absence abolish the asexual reproduction of Z. tritici. 42Taken together, our data show that ZtSo is required for fungal development, while 43 vegetative cell fusions are essential for fungal fitness. 44 45 46 47 48 49 50

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Section: Discussionsupporting

confidence: 91%

“…Z. tritici alters its growth morphology in detrimental to the nutritional conditions (Francisco et al , 2019). To assess whether vegetative cell fusion affects fungal growth, we determined the radial growth of ΔZtKu70, ΔZtSo, and ΔZtSo -comp on different culture media.…”

Section: Resultsmentioning

confidence: 99%

The role of vegetative cell fusions in the lifestyle of the wheat fungal pathogenZymoseptoria tritici

Francisco¹,

Zwyssig²,

Palma‐Guerrero³

2020

Preprint

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“…The differences in carrying capacity for the ∆ Zt107320 strains could be indicative of an earlier nutrient limitation due to lower efficiency in nutrient usage. This nutrient limitation could therefore be responsible for the more pronounced switch to hyphal growth, in particular, since carbon limitation increases mycelial growth (Francisco et al , ). This is further supported by the fact that 24 h after inoculation onto solid MM no differences in growth pattern were observable between the wild type, the Zt107320 deletion and complementation strains (data not shown).…”

Section: Discussionmentioning

confidence: 99%

The transcription factor Zt107320 affects the dimorphic switch, growth and virulence of the fungal wheat pathogen Zymoseptoria tritici

Habig

Bahena-Garrido

Barkmann

et al. 2019

Molecular Plant Pathology

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Summary Zymoseptoria tritici is a filamentous fungus causing Septoria tritici blotch in wheat. The pathogen has a narrow host range and infections of grasses other than susceptible wheat are blocked early after stomatal penetration. During these abortive infections, the fungus shows a markedly different gene expression pattern. However, the underlying mechanisms causing differential gene expression during host and non‐host interactions are largely unknown, but likely include transcriptional regulators responsible for the onset of an infection programme in compatible hosts. MoCOD1, a member of the fungal Zn(II)2Cys6 transcription factor family, has been shown to directly affect pathogenicity in the rice blast pathogen Magnaporthe oryzae. Here, we analyse the role of the putative transcription factor Zt107320, a homologue of MoCOD1, during infection of compatible and incompatible hosts by Z. tritici. We show for the first time that Zt107320 is differentially expressed in host versus non‐host infections and that lower expression corresponds to an incompatible infection of non‐hosts. Applying reverse genetics approaches, we further show that Zt107320 regulates the dimorphic switch as well as the growth rate of Z. tritici and affects fungal cell wall composition in vitro. Moreover, ∆Zt107320 mutants showed reduced virulence during compatible infections of wheat. We conclude that Zt107320 directly influences pathogen fitness and propose that Zt107320 is involved in the regulation of growth processes and pathogenicity during infection.

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“…For isolates 1A5, 1E4, 3D1 and 3D7, RNA sequencing experiments on minimal media were performed by [45,67]. Raw reads were retrieved from the NCBI Short Read Archive accession number SRP077418.…”

Section: Rna Extraction Library Preparation Sequencing and Quantifimentioning

confidence: 99%

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

et al. 2020

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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.

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Morphological changes in response to environmental stresses in the fungal plant pathogen Zymoseptoria tritici

Cited by 94 publications

References 86 publications

The role of vegetative cell fusions in the lifestyle of the wheat fungal pathogenZymoseptoria tritici

The role of vegetative cell fusions in the lifestyle of the wheat fungal pathogenZymoseptoria tritici

The transcription factor Zt107320 affects the dimorphic switch, growth and virulence of the fungal wheat pathogen Zymoseptoria tritici

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

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