Facilitation of symplastic effector protein mobility by paired effectors is conserved in different classes of fungal pathogens

Abstract

Recently, it was uncovered that plant pathogens produce effectors that spread via plasmodesmata to allow modulation of host processes in distal uninfected cells. Fusarium oxysporum forma specialis lycopersici (Fol) facilitates effector translocation by expansion of the size exclusion limit of plasmodesmata using the Six5/Avr2 effector pair. How other fungal pathogens manipulate plasmodesmata is unknown. We recently reported that many fungal pathogens belonging to different families carry effector pairs that resemble the SIX5/AVR2 gene pair from Fol. Here, we performed structural predictions of three of these effector pairs from Leptosphaeria maculans (Lm) and tested their ability to manipulate plasmodesmata and to complement the virulence defect of a Fol SIX5 knockout mutant. We show that the AvrLm10A homologs are structurally related to FolSix5 and localize at plasmodesmata when they are expressed with their paired effector. Furthermore, these effectors were found to complement FolSix5 function in cell-to-cell mobility assays and in fungal virulence. We conclude that distantly related fungal species rely on structurally related paired effector proteins to manipulate plasmodesmata and facilitate effector mobility. The wide distribution of these effector pairs implies Six5-mediated effector translocation to be a conserved propensity among fungal plant pathogens.