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.
Highlights
Diverse groups of pathogenic fungi threaten plant health, whereas certain fungi, such as endophytes and mycorrhizal fungi, allow plants to explore new niches, manage biotic and abiotic stresses better, and/or efficiently acquire key nutrients
We developed a pipeline for mining small secreted proteins (SSPs) as effector candidates from fungi with different lifestyles and taxonomic positions in order to conduct their kingdom-wide comparative analysis
It has been commonly hypothesized that biotrophs and symbionts secrete more effectors than necrotrophs, as biotrophic associations require the modulation of the host defense system to keep host cells alive for nutrient acquisition while preventing the launch of strong defense responses
Summary
Diverse groups of pathogenic fungi threaten plant health, whereas certain fungi, such as endophytes and mycorrhizal fungi, allow plants to explore new niches, manage biotic and abiotic stresses better, and/or efficiently acquire key nutrients. Analysis of the size of secretome relative to the total proteome in 48 fungal species by Lowe and Howlett (2012) suggested its potential relationship with lifestyles Another comparative study by Meinken et al (2014) proposed that the secretome prediction of previous study may be overestimated because only SignalP was used for the prediction, but they drew the same conclusion. The study by Krijger et al (2014) suggested that phylogenetic position strongly influenced both the secretome size and its composition by analyzing 33 fungal species but did not include major secreted enzyme groups In addition those displaying different modes of pathogenesis (biotroph, hemibiotroph, and necrotroph) were combined as a single lifestyle in the last two analyses. To investigate whether the composition and size of putative effectors correlates with different lifestyles, such enzymes should be analyzed separately
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