ABSTRACT
Ectomycorrhizal fungi (EMF) grow as saprotrophs in soil and interact with plants, forming mutualistic associations with roots of many economically and ecologically important forest tree genera. EMF ensheath the root tips and produce an extensive extramatrical mycelium for nutrient uptake from the soil. In contrast to other mycorrhizal fungal symbioses, EMF do not invade plant cells but form an interface for nutrient exchange adjacent to the cortex cells. The interaction of roots and EMF affects host stress resistance but uncovering the underlying molecular mechanisms is an emerging topic. Here, we focused on local and systemic effects of EMF modulating defenses against insects or pathogens in aboveground tissues in comparison with arbuscular mycorrhizal induced systemic resistance. Molecular studies indicate a role of chitin in defense activation by EMF in local tissues and an immune response that is induced by yet unknown signals in aboveground tissues. Volatile organic compounds may be involved in long-distance communication between below- and aboveground tissues, in addition to metabolite signals in the xylem or phloem. In leaves of EMF-colonized plants, jasmonate signaling is involved in transcriptional re-wiring, leading to metabolic shifts in the secondary and nitrogen-based defense metabolism but cross talk with salicylate-related signaling is likely. Ectomycorrhizal-induced plant immunity shares commonalities with systemic acquired resistance and induced systemic resistance. We highlight novel developments and provide a guide to future research directions in EMF-induced resistance.
ABSTRACT
The unfolded protein response (UPR), a conserved eukaryotic signaling pathway to ensure protein homeostasis in the endoplasmic reticulum (ER), coordinates biotrophic development in the corn smut fungus Ustilago maydis. Exact timing of UPR activation is required for virulence and presumably connected to the elevated expression of secreted effector proteins during infection of the host plant Zea mays. In the baker's yeast Saccharomyces cerevisiae, expression of UPR target genes is induced upon binding of the central regulator Hac1 to unfolded protein response elements (UPREs) in their promoters. While a role of the UPR in effector secretion has been described previously, we investigated a potential UPR-dependent regulation of genes encoding secreted effector proteins. In silico prediction of UPREs in promoter regions identified the previously characterized effector genes pit2 and tin1-1, as bona fide UPR target genes. Furthermore, direct binding of the Hac1-homolog Cib1 to the UPRE containing promoter fragments of both genes was confirmed by quantitative chromatin immunoprecipitation (qChIP) analysis. Targeted deletion of the UPRE abolished Cib1-dependent expression of pit2 and significantly affected virulence. Furthermore, ER stress strongly increased Pit2 expression and secretion. This study expands the role of the UPR as a signal hub in fungal virulence and illustrates, how biotrophic fungi can coordinate cellular physiology, development and regulation of secreted virulence factors.
