Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles

Abstract

Zymoseptoria tritici causes Septoria tritici blotch (STB) on wheat. The disease interaction is characterized by clearly defined temporal phases of infection, ultimately resulting in the death of host tissue. Zymoseptoria tritici is a highly polymorphic species with significant intraspecific variation in virulence profiles. We generated a deep transcriptomic sequencing dataset spanning the entire time course of an infection using a previously uncharacterized, highly virulent Z. tritici strain isolated from a Swiss wheat field. We found that seven clusters of gene transcription profiles explained the progression of the infection. The earliest highly up-regulated genes included chloroperoxidases, which may help the fungus cope with plant defences. The onset of necrotrophy was characterized by a concerted up-regulation of proteases, plant cell wall-degrading enzymes and lipases. Functions related to nutrition and growth characterized late necrotrophy and the transition to saprotrophic growth on dead plant tissue. We found that the peak up-regulation of genes essential for mating coincided with the necrotrophic phase. We performed an intraspecies comparative transcriptomics analysis using a comparable time course infection experiment of the genome reference isolate IPO323. Major components of the fungal infection transcriptome were conserved between the two strains. However, individual small, secreted proteins, proteases and cell wall-degrading enzymes showed strongly differentiated transcriptional profiles between isolates. Our analyses illustrate that successful STB infections involve complex transcriptomic remodelling to up-regulate distinct gene functions. Heterogeneity in transcriptomes among isolates may explain some of the considerable variation in virulence and host specialization found within the species.

The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

“…We combined two types of evidence to guide the predictions, as follows: (i) we mapped protein sequences of isolate IPO323 (33) to the genome of 3D7, and (ii) we identified transcript locations using two deep-RNA-sequencing datasets generated for the complete infection cycle of 3D7 (41). We identified a total of 11,737 genes in 3D7.…”

“…5G). Finally, we analyzed previously generated transcriptomics data over the entire time course of a wheat infection (41) to determine gene expression levels and identify differential regulation. The core secretome contained a large number of genes that were upregulated during infection (see Fig.…”

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

“…To annotate the other genes in the cluster, we used RNA‐seq raw data of 3D7 from two different experiments and at six different time points (Palma‐Guerrero et al ., 2016). The data were previously deposited in NCBI with experiment numbers SRP061444 and ERP009837.…”

Durum wheat and septoria tritici blotch: genes and prospects for breeding

“…Despite the macoscopical lack of symptoms, microscopic observations by showed that chloroplasts are in constant move towards the cell wall during this phase, which suggests that Z. tritici acts on the plant cell physiology by altering its functionality. The release of small secreted proteins may explain these observations (Ben M'Barek et al 2015;Gohari 2015;Kettles et al 2017;Mirzadi Gohari et al 2015;Palma-Guerrero et al 2016;Rudd et al 2015), and contrary to other ascomycete cereal pathogens, Z. tritici also encodes a few carbohydrate-active enzyme family proteins, but abundant peptidase and alpha-amylase enzymes, which suggests an alternative nutrient acquisition of Z. tritici from its host environment (Fones et al 2017;). Moreover, genes encoding for lipases, cutinases and fatty acid metabolism enzymes are up-regulated during this phase (Keon et al 2007;Palma-Guerrero et al 2017;Rudd et al 2015), which suggests that Z. tritici relies upon stored energy in germinating spores that are conceivably supplemented by cuticular waxes rather than tapping directly from host resources (Kettles et al 2017;Rudd et al 2015).…”

“…Moreover, genes encoding for lipases, cutinases and fatty acid metabolism enzymes are up-regulated during this phase (Keon et al 2007;Palma-Guerrero et al 2017;Rudd et al 2015), which suggests that Z. tritici relies upon stored energy in germinating spores that are conceivably supplemented by cuticular waxes rather than tapping directly from host resources (Kettles et al 2017;Rudd et al 2015). Host defence mechanisms are most probably supressed during this latent phase (Hammond-Kosack and Rudd 2008;Palma-Guerrero et al 2016;Rudd 2015). The secretion of LysM effectors by Z. tritici prevents chitin recognition, which also supports its invasion and one LysM effector plays a role in virulence, suggesting various roles of these effectors (Lee et al 2014;Marshall et al 2011).…”