Rumble in the Effector Jungle: Candidate Effector Proteins in Interactions of Plants with Powdery Mildew and Rust Fungi

Abstract

Rust and powdery mildew fungi are widespread obligate biotrophic phytopathogens. They colonize a broad range monocotyledonous and dicotyledonous host plant species and in the case of crop plants can cause severe yield losses. While powdery mildews (Ascomycota) grow mainly epiphytically and infect the host epidermis, rust fungi (Basidiomycota) typically enter host tissues through stomata and spread within the intercellular spaces. Both fungal taxa have unusually large genomes that are rich in repetitive elements (mostly derived from retrotransposons) and experienced a convergent loss of genes usually present in free-living fungi compared to their respective relatives. Genomes of rust and powdery mildew fungi encode many candidates for secreted effector proteins thought to aid the suppression of defense and cell death or to mediate nutrient acquisition. Although the precise biochemical activity of most effector proteins remains obscure, candidate host targets have been identified for several of them. In addition, some effectors are perceived by matching plant immune receptors and thus serve as avirulence determinants in plant-fungus interactions. This review article summarizes the current knowledge of rust and powdery mildew effector proteins and raises and discusses urgent questions regarding future research. Abbreviations: AVR: avirulence protein; BiFC: bimolecular fluorescence complementation; CSEP: candidate secreted effector protein; ETI: effector-triggered immunity; f. sp.: forma specialis; ff. spp.: formae speciales; MS: mass spectrometry; RIP: repeat-induced point mutation; R protein: resistance protein; sRNA: small RNA; TE: transposable element; Y2H: yeast-2-hybrid.