Effector discovery in the fungal wheat pathogen Zymoseptoria tritici

Abstract

Fungal plant pathogens, such as Zymoseptoria tritici (formerly known as Mycosphaerella graminicola), secrete repertoires of effectors to facilitate infection or trigger host defence mechanisms. The discovery and functional characterization of effectors provides valuable knowledge that can contribute to the design of new and effective disease management strategies. Here, we combined bioinformatics approaches with expression profiling during pathogenesis to identify candidate effectors of Z. tritici. In addition, a genetic approach was conducted to map quantitative trait loci (QTLs) carrying putative effectors, enabling the validation of both complementary strategies for effector discovery. In planta expression profiling revealed that candidate effectors were up-regulated in successive waves corresponding to consecutive stages of pathogenesis, contrary to candidates identified by QTL mapping that were, overall, expressed at low levels. Functional analyses of two top candidate effectors (SSP15 and SSP18) showed their dispensability for Z. tritici pathogenesis. These analyses reveal that generally adopted criteria, such as protein size, cysteine residues and expression during pathogenesis, may preclude an unbiased effector discovery. Indeed, genetic mapping of genomic regions involved in specificity render alternative effector candidates that do not match the aforementioned criteria, but should nevertheless be considered as promising new leads for effectors that are crucial for the Z. tritici-wheat pathosystem.

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

“…It is possible that the role of Avr3D1 is more pronounced under field conditions or at different developmental stages, for example in adult plants. An additional hypothesis to explain the apparent dispensability of Avr3D1 is that functional redundancy masks phenotypic effects in the knockout mutants (Marshall et al ., 2011; Win et al ., 2012; Mirzadi Gohari et al ., 2015; Rudd et al ., 2015). …”

Is Zymoseptoria tritici a hemibiotroph?

“…Disruption of several of these effector candidate genes has shown that they are not essential for virulence. This may indicate functional redundancy or a major role in necrosis induction for other molecular players such as secondary metabolites, toxins and/or cell wall degrading enzymes (Gohari et al, 2015;Rudd et al, 2015). It was also suggested that programmed cell death is triggered by the pathogen at the onset of the necrotrophic phase (Keon et al, 2007).…”

“…Environmental stresses such as light, water availability and temperature fluctuations may play a role, but the switch may also be linked to pathogen conditions or host developmental signals. Z. tritici probably uses several mechanisms to induce necrosis, including the production of protein effectors (Brunner et al, 2013;Gohari et al, 2015;Keon et al, 2007;Rudd et al, 2008;Rudd et al, 2015). In fact, several genes encoding small cysteine rich proteins are highly expressed during the necrotrophic phase.…”

Proteome catalog of Zymoseptoria tritici captured during pathogenesis in wheat

“…Here, we identified 12 secreted cysteine-rich proteins (3-10 cysteine residues) of which nine were small secreted proteins (SSPs) (less than 300 amino acids, Mirzadi Gohari et al, 2015). Several SSPs have shown to exhibit effector functions in various pathosystems (Rep, 2005;Houterman et al, 2007;Bolton et al, 2008).…”