Leveraging genomics to understand the broader role of fungal small secreted proteins in niche colonization and nutrition

Abstract

The last few years have seen significant advances in the breadth of fungi for which we have genomic resources and our understanding of the biological mechanisms evolved to enable fungi to interact with their environment and other organisms. One field of research that has seen a paradigm shift in our understanding concerns the role of fungal small secreted proteins (SSPs) classified as effectors. Classically thought to be a class of proteins utilized by pathogenic microbes to manipulate host physiology in support of colonization, comparative genomic studies have demonstrated that mutualistic fungi and fungi not associated with a living host (i.e., saprotrophic fungi) also encode inducible effector and candidate effector gene sequences. In this review, we discuss the latest advances in understanding how fungi utilize these secreted proteins to colonize a particular niche and affect nutrition and nutrient cycles. Recent studies show that candidate effector SSPs in fungi may have just as significant a role in modulating hyphosphere microbiomes and in orchestrating fungal growth as they do in supporting colonization of a living host. We conclude with suggestions on how comparative genomics may direct future studies seeking to characterize and differentiate effector from other more generalized functions of these enigmatic secreted proteins across all fungal lifestyles.

Genomic innovation and horizontal gene transfer shaped plant colonization and biomass degradation strategies of a globally prevalent fungal pathogen

“…These data indicate that certain proteins of A. luteobubalina can cause necrotic lesions in host plant tissue. The evolutionary conservation of these two proteins outside Armillaria is somewhat surprising and is in contrast with observations on other (mostly Ascomycota) effectors 46,47 .…”

“…Small secreted proteins (SSPs), which include cysteine-rich proteins involved in, among others, host colonization 46 , were found in 270-507 copies in Armillaria , with A. fuscipes having the fewest and A. luteobubalina having the most. Of these, 45-57% had no known functional domains, which we hereafter refer to as unannotated SSPs.…”

Sesquiterpenes of the ectomycorrhizal fungus Pisolithus microcarpus alter root growth and promote host colonization

“…While we do not know the mechanism of this repression, nor was there a mechanism proposed by Nones et al ( 2022 ), a recent study on the interaction of Populus with L. bicolor suggests that fungal-secreted proteins may control plant terpene production (Marques-Galvez et al 2022 ). Plant-interacting fungi release a suite of small secreted proteins that alter plant physiology and promote symbiosis (Plett and Plett 2022 ; Snelders et al 2022 ). One of these, LbMiSSP7, produced by L. bicolor, interacts with a host jasmonic acid (JA) co-receptor, which represses JA-induced gene transcription (Daguerre et al 2020 ; Plett et al 2014 ).…”

Snowball: a novel gene family required for developmental patterning in fruiting bodies of mushroom-forming fungi (Agaricomycetes)

“…Unannotated genes in fungal genomes are frequently highly variable and encode effectors or small secreted proteins. Examples of recently characterized such gene families include mycorrhiza-induced small secreted proteins (92), a short Cryptococcus neoformans peptide related to quorum sensing (93), effector-like Ssp1 from Pleurotus ostreatus (94), or a cell-surface effector complex from Ustilago (95), among others. However, not all unannotated genes lack conservation.…”