Abstract
Phytopathogenic ascomycete fungi possess huge effector repertoires that are dominated by hundreds of sequence-unrelated small secreted proteins. The molecular function of these effectors and the evolutionary mechanisms that generate this tremendous number of singleton genes are largely unknown. To get a deeper understanding of fungal effectors, we determined by NMR spectroscopy the 3-dimensional structures of the Magnaporthe oryzae effectors AVR1-CO39 and AVR-Pia. Despite a lack of sequence similarity, both proteins have very similar 6 β-sandwich structures that are stabilized in both cases by a disulfide bridge between 2 conserved cysteins located in similar positions of the proteins. Structural similarity searches revealed that AvrPiz-t, another effector from M. oryzae, and ToxB, an effector of the wheat tan spot pathogen Pyrenophora tritici-repentis have the same structures suggesting the existence of a family of sequence-unrelated but structurally conserved fungal effectors that we named MAX-effectors (M agnaporthe Avrs and ToxB like). Structure-informed pattern searches strengthened this hypothesis by identifying MAX-effector candidates in a broad range of ascomycete phytopathogens. Strong expansion of the MAX-effector family was detected in M. oryzae and M. grisea where they seem to be particularly important since they account for 5–10% of the effector repertoire and 50% of the cloned avirulence effectors. Expression analysis indicated that the majority of M. oryzae MAX-effectors are expressed specifically during early infection suggesting important functions during biotrophic host colonization. We hypothesize that the scenario observed for MAX-effectors can serve as a paradigm for ascomycete effector diversity and that the enormous number of sequence-unrelated ascomycete effectors may in fact belong to a restricted set of structurally conserved effector families.
Highlights
Pathogenic microorganisms have to cope with the immune system of their host and deploy measures to hide their presence, disturb host immunity or inactivate defense responses
Phytopathogenic fungi possess huge effector repertoires that are dominated by hundreds of sequence-unrelated small secreted proteins
By investigating the 3-dimensional structures of effectors from the rice blast fungus M. oryzae, we discovered an effector family comprising structurally conserved but sequence-unrelated effectors from M. oryzae and the phylogenetically distant wheat pathogen Pyrenophora tritici-repentis that we named MAX-effectors (M. oryzae Avrs and ToxB)
Summary
Pathogenic microorganisms have to cope with the immune system of their host and deploy measures to hide their presence, disturb host immunity or inactivate defense responses. The vast majority of the fungal effectors do not share sequence similarities with other proteins and do not contain conserved motifs This is very different from the situation in other phytopathogens and in particular oomyctes, an important class of plant pathogens that have similar lifestyles and infection strategies and whose virulence relies on large effector repertoires. Effector repertoires dominated by gene families of large size counting more than 5 members were only detected in particular cases such as powdery mildew and rust fungi lineages [10,11,12,13] Due to their high diversity and the lack of similarity with other proteins, the mode of action and the role in infection of fungal effectors have to be elucidated case by case and remain still largely unknown [5,6]. This tremendous diversity raises the question of the evolutionary trajectories of fungal effectors that do not show traces of common origins
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