Kingdom-Wide Analysis of Fungal Small Secreted Proteins (SSPs) Reveals their Potential Role in Host Association

Abstract

Fungal secretome consists of various functional groups of proteins, many of which participate in nutrient acquisition, self-protection, or manipulation of the environment and neighboring organisms. The least characterized component of the secretome is small secreted proteins (SSPs). Some SSPs have been reported to function as effectors, but most remain to be characterized. The composition of major secretome components, such as carbohydrate-active enzymes, proteases, lipases, and oxidoreductases, appear to reflect the lifestyle and ecological niche of individual species. We hypothesize that many SSPs participate in manipulating plants as effectors. Obligate biotrophs likely encode more and diverse effector-like SSPs to suppress host defense compared to necrotrophs, which generally use cell wall degrading enzymes and phytotoxins to kill hosts. Because different secretome prediction workflows have been used in different studies, available secretome data are difficult to integrate for comprehensive comparative studies to test this hypothesis. In this study, SSPs encoded by 136 fungal species were identified from data archived in Fungal Secretome Database (FSD) via a refined secretome workflow. Subsequently, compositions of SSPs and other secretome components were compared in light of taxa and lifestyles. Those species that are intimately associated with host cells, such as biotrophs and symbionts, usually have higher proportion of species-specific SSPs (SSSPs) than hemibiotrophs and necrotrophs, but the latter groups displayed higher proportions of secreted enzymes. Results from our study established a foundation for functional studies on SSPs and will also help understand genomic changes potentially underpinning different fungal lifestyles.

Growing evidence for facultative biotrophy in saprotrophic fungi: data from microcosm tests with 201 species of wood‐decay basidiomycetes

“…The development of Hartig net‐like structures by P. igniarius thus suggests the use of effectors such as MiSSP7 and potentially constitutes an independent ECM symbiotic origin event. Although secretomic analysis indicates that wood‐decay fungi produce a reduced complement of effector proteins compared with obligate biotrophs (Kim et al ., ), P. igniarius in particular has not been examined, and to our knowledge no transcriptomic or secretomic analysis has been carried out using saprotrophic fungi grown with seedlings as in the present study.…”

Conservation and expansion of a necrosis‐inducing small secreted protein family from host‐variable phytopathogens of the Sclerotiniaceae

“…GenBank BLAST annotations and BLAST2GO enzyme codes were used to manually group the proteins into 32 common categories (Table ). Proteins were conservatively annotated as SSPs if they were shorter than 200 amino acids in length and had ≥4% cysteine content (Kim et al , ).…”

Apoplastic fungal effectors in historic perspective; a personal view

“…The secretome of plant‐pathogenic fungi represents, on average, c . 10% of the proteins encoded in their genomes, but these numbers may vary depending on their lifestyle (Kim et al ., ). HR‐inducing Avr activities of secreted proteins are easy to score on resistant host plants, but their virulence functions are more difficult to score, especially when their contribution to virulence is small.…”

“…. Currently, kingdom‐wide comparisons of fungal secretomes are being performed to search for different types of secreted Avr factor and enzyme (Kim et al ., ). Avrs are often species‐specific and very diverse in sequence; sometimes effectors show strong structural conservation, which might help in the search for functionally conserved homologs in diverse fungal pathogens (De Jonge et al ., ; Stergiopoulos et al ., ; De Guillen et al ., ).…”

“…Some biotrophic and hemibiotrophic pathogens, including U. maydis , have evolved effectors to down‐regulate the plant defense hormone salicylic acid (Tanaka et al ., ). Many more enzyme effectors are encoded by fungal genomes, but their role in virulence still needs to be determined (Kim et al ., ).…”