Fungal effectors: past, present, and future

Abstract

Fungal effector proteins function at the interfaces of diverse interactions between fungi and their plant and animal hosts, facilitating interactions that are pathogenic or mutualistic. Recent advancements in protein structure prediction have significantly accelerated the identification and functional predictions of these rapidly evolving effector proteins. This development enables scientists to generate testable hypotheses for functional validation using experimental approaches. Research frontiers in effector biology include understanding pathways through which effector proteins are secreted or translocated into host cells, their roles in manipulating host microbiomes, and their contribution to interacting with host immunity. Comparative effector repertoires among different fungal-host interactions can highlight unique adaptations, providing insights for the development of novel antifungal therapies and biocontrol strategies.

Figure 1.. Fungal conserved mechanisms of host colonization depicted in a plant cell.

Depicted is a fungal hypha colonizing the apoplastic space of a plant cell, with examples of apoplastic and cytoplasmic secreted effectors and their host targets. Apoplastic effectors may function to 1) evade chitin-triggered plant immunity recognition, 2) degrade plant cell wall or, 3) bind to host proteins to change microenvironment or alter host defenses and promote colonization. Cytoplasmic effectors may localize to subcellular compartments to 4) perturb defense signaling pathways through mitochondria or chloroplasts, 5) reprogram transcription, or 6) target or mimic host proteasome machinery to regulate plant immune responses.

Figure 2.. Host-fungal interactions are illustrated using Fusarium oxysporum species complex.

A cross-kingdom fungal pathogen, members within the F. oxysporum species complex include a) plant pathogens that cause vascular wilt diseases in many economically important plants, as illustrated using the model plant Arabidopsis thaliana, b) the endophytic strains that provide protective advantages to host plants and promote plant growth; and c) human pathogens that repress mammalian immunity and cause systematic infections. d) Whole genome comparison among three F. oxysporum genomes that represent a plant pathogen (Fo4287 in blue), an endophytic strain (Fo47 in green) and a human pathogen (FoMRL8996 in orange). All three genomes share 11 conserved core chromosomes, while each carries unique set of accessory chromosomes highlighted in darker shades in each genome (i) with low gene density (ii) that contributed to the unique host-specific interactions. The inner circle indicates syntenic alignments using Nucmer. (Xy: Xylem vassel, Pc: Pericyde, Ed: Endodermis, Cx: Cortex, Ep: Epidermis, Mp: Macrophage, Bs: Bloodstream). a) and b) were adopted from Martínez-Soto D et al https://doi.org/2023 10.1094/MPMI-08-22-0166-SC and c) was based on https://doi.org/10.1371/journal.pone.0101999