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Animals must tailor their life-history strategies to suit the prevailing conditions and respond to hazards in the environment. Animals with lethal infections are faced with a difficult choice: to allocate more resources to reproduction and suffer higher mortality or to reduce reproduction with the expectation of enhanced immunity and late-age reproduction. However, the strategies employed to mediate shifts in life-history traits are largely unknown.


They are characteristically shorter than amino acids in length and have a al peptide. The majority of SSPs are coded by orphan genes, which lack known domains or similarities to known protein sequences. Effectors are a group of SSPs that have been investigated extensively in fungi that interact with living hosts, either pathogens or mutualistic systems. They are involved in suppressing the host defense response and altering its physiology.

The effector-like Ssp1 from the white-rot fungus Pleurotus ostreatus is presented as a case study, and its potential role in regulating the ligninolytic system, secondary metabolism, development, and fruiting body initiation are discussed.

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We propose that deciphering the nature of effector-like SSPs will contribute to our understanding of development and communication in saprophytic fungi, as well as help, to elucidate the origin, regulation, and mechanisms of fungal-host, fungal-fungal, and fungal-bacterial interactions. The success of fungi to adapt and proliferate in diverse ecological niches is dependent on their ability to respond to changes in the environment.

The rich, yet versatile, fungal secretome is an important component that facilitates the fast adjustment to changes occurring in the vicinity of the growing and developing fungus Krijger et al. Nonetheless, the composition of fungal secretomes can be extremely variable, even within the same fungal species and under similar environmental conditions Girard et al.

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The secretome is composed of proteins that participate in organic matter degradation, such as proteases, lipases, Carbohydrate-Active enZymes CAZymesbut also hydrophobins and small-secreted proteins SSPs Alfaro et al. SSPs are secreted by fungi independently of their lifestyle and are defined as proteins that contain a al peptide and a sequence of less than amino acids. Here, we follow the common paradigm defining effectors as SSPs used by a range of pathogenic and beneficial fungi to alter the physiological status of the host plant Veneault-Fourrey and Martin, ; Win et al.

We specifically focus on SSPs in fungi that exhibit predominantly saprotrophic lifestyles and can be bioinformatically classified as effector Sperschneider et al. Others have already suggested that effector-like proteins may have yet undiscovered roles in saprophytic growth, nutrition and development Girard et al. SSPs functioning as effectors are common in several plant pathogens Lo Presti et al.

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Many effectors have weak or no sequence similarity to proteins with known activity, and only some of them are considered conserved. Nonetheless, more recent studies have revealed that effectors probably share more structural conservation, which is less evident on the basis of their primary sequences Lo Presti et al. One proposed explanation for this is that they are under strong selective pressure which has led to their accelerated divergent evolution Carvunis et al.

Some effector families were probably expanded by duplication and diversification from a common ancestor, or through horizontal gene transfer Lo Presti et al. One criterion for classifying effectors is based on their localization in the host. They are considered either apoplastic localize to the apoplast or cytoplasmic enter into the plant cells Lo Presti et al.

Seeking the roles for fungal small-secreted proteins in affecting saprophytic lifestyles

Their translocation into the plant cells is still poorly understood Lo Presti and Kahmann, The content of small secreted cysteine-rich proteins, usually classified as effectors, is relatively close between saprophytes and plant pathogens, and lower in animal pathogens Krijger et al. Genomic adaptation of effectors was strongly linked to fungal pathogens -host interactions, for both plants and animals, suggesting gene-for-gene relationships is also prevalent in fungus—animal interactions Shang et al.

In the example of the nematode-trapping fungus Duddingtonia flagranseffectors were predicted, of which PefB was induced during interaction with the host and was imported into host nuclei in vitro Youssar et al.

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A symbiotic lifestyle requires an inducible ability to control plant defenses, a function attributed to mycorrhiza-induced small secreted proteins MiSSPs Plett et al. The best-studied example is MiSSP7 in Laccaria bicolorwhich is upregulated in ectomycorrhizal root tips Martin et al.

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It is secreted into the extracellular environment after sensing of diffusible plant als and immediately translocated into the root. In plantaMiSSP7 manipulates the co-receptor of jasmonate and related aling pathways of the host, to initiate fungal colonization Plett et al.

MiSSP8 has a fungal-specific repetitive motif, present not only in ectomycorrhizal but also in saprotrophic SSPs, and might also be relevant for fruiting body formation Pellegrin et al. The Rhizophagus irregularis SP7 protein, manipulates the ethylene-aling pathway and is localized to the host nucleus where it subsequently reshuffles plant defense pathways Kloppholz et al. Gene expression analyses of Cenococcum geophilum interacting with different hosts were used to identify MiSSPs and showed that six of them are targeted to distinct subcellular compartments in planta de Freitas Pereira et al.

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The fact that SSPs have been found in the genomes of plants that host mycorrhizal fungi Yang et al. In Populus trichocarpaeffector-like SSPs are upregulated during symbiotic interactions.

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They have been shown to enter L. Another example of SSPs are hydrophobins are present across the fungal kingdom and have an ability to self-assemble into films at hydrophilic-hydrophobic interfaces Wessels, ; Bayry et al. They have been found to be regulated during development of the ectomycorrhizal basidiomycete Tricholoma vaccinum and differentially expressed during the early steps of mycorrhization, in a manner that is dependent on host preference Sammer et al. In saprotrophic fungi, SSPs can be involved in degradative capabilities like in the case of Trichoderma reesei swollenin, which depolymerizes cellulose Saloheimo et al.

SSPs could also recruit enzymes at the surface of the substrate or interact with enzymes to increase their activity. For example, HsbA in Aspergillus oryzae has been demonstrated to recruit lytic enzymes to the surface of hydrophobic solid materials Ohtaki et al.

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In an analysis comparing secretion patterns of SSPs in 8 Aspergillus spp. Other SSPs were suggested to be a part of the fungal stress response to the toxicity of several aromatic compounds or reactive oxygen species released during biomass degradation Valette et al. The EffectorP 2. Genomic comparisons between pathogenic and saprophytic species were used to reveal the differences between fungi exhibiting the two lifestyles, unveiling an intriguing role of the effector repertoires.

The genomic effector range of activity in the saprophytic fungus Verticillium tricorpus resembles that of its plant pathogenic relative V. Genome-wide analysis of the transition to pathogenic lifestyles in Magnaporthales showed that pathogens had more clade-specific SSPs than the wood-inhabiting non-pathogenic clade. Some of the effectors were specific to the pathogenic clade and are likely to play key roles in the interaction with the host, but some were conserved with those of the saprophytic members Zhang et al.

In Fusarium spp. King et al. Another example is the large arsenal of effectors in Pseudozymasaprotrophic yeasts, which has been suggested to have originated from an unknown plant pathogenic stage required for sexual recombination Sharma et al.

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Cerato-platanin proteins are believed to be important for plant-fungal interactions but are also present in saprophytes such as Trichoderma Kubicek et al. In Phlebia radiataan efficient plant cell wall decomposer, genes coding for SSPs were found, 83 of which were also identified by EffectorP SSPs may also be involved in fungal-bacterial interactions.

SSP gene expression was reported to be induced during interactions between Podospora anserina and Serratia species Lamacchia et al. The genome of the P. Interestingly, some families such as ricin-B-lectin and hydrophobins are conserved in Pleurotus like in most fungi included in the analysis.

Our analysis is biased toward predicted effectors found in the proteome of Pleurotus, a saprophytic WRF, thus excluding pathogens or ectomycorrhizal specific effectors, hence no apparent clades according to life-style occurred Supplementary Figure S1. On the other hand the four representative of the Ascomycota, comprise a different clade. Similar upregulation occurred after exposure to several other aryl-alcohols as well as during idiophase after the onset of secondary metabolism Feldman et al. Ssp1 was also the most upregulated gene, up to fold, during interspecific interactions between P.

Homologs of poSSPs were found in 22 fungal species.

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Among them, 16 members of the order Agaricales and 3 of Auriculariales. Most of these are basidiomycota and only 3 representatives of the ascomycota were found. A majority of these fungi harbor multiple, highly similar, copies of Ssp1-coding genes Table 1. This may suggest that the genomic origin of these SSPs is from the Agaricales, and the multiple copies were generated through duplication events.

The wealth of information accumulated concerning the physiology of P. Reverse genetics was used to elucidate the function of Ssp1, by using RNAi to knockdown expression of the entire family KD ssp1 or by overexpression of the dominant Ssp1 member OE ssp 1 Feldman et al.

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Analysis of the phenotypes revealed an interesting role of Ssp1 in the regulation of development. The mutations in Ssp1 conferred a time shift in their secretion and expression patterns; OE ssp1 entered the idiophase earlier, accompanied by the formation of yellow pigment and faster aging.

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In contrast, the KD ssp1 had a longer tropohase, the strain did not generate pigmentation and no lysis of the colony occurred. Taken together, Ssp1 was shown to be involved in the transition from tropohase to idiophase, aging, and metabolism Feldman et al. Overexpression of Ssp1 also negatively affected fruiting body initiation Feldman et al.

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It seems that different poSSPs are regulated and produced under diverse conditions. Ssp were produced in rich peptone-glucose media and following exposure to HMF Feldman et al. However, Ssp6 was produced in cellulose-based media Yoav et al. SSPs are a ificant, yet still a functionally-elusive, part of the fungal secretome, especially in saprophytes. Nonetheless, some of them are the likely ancestors of the better understood effectors in pathogenic and mutualistic fungi Seidl et al. Part of the enigma concerning the role of SSPs in saprophytes is based on the alleged contradiction that effector-like SSPs are a considerable component of their secretome, yet, these organisms obtain nutrients directly from dead organic matter without forming interactions with a living host.

This raises the question — whom do these effector-like proteins affect? One tempting conclusion is that SSPs participate in the ability of these fungi to grow in a specific ecological niche, yet in a completely unrelated fashion to that elucidated for pathogens. One form of microbial communication is quorum sensing QS Miller and Bassler, In fungi, QS has been described to regulate processes such as sporulation, secondary metabolite production, morphological transition and enzyme secretion Barriuso et al. The effects of Ssp1 in P. The majority of the known fungal QS molecules are chemical compounds, such as farnesol and alcohol tyrosol, like in Candida albicans Albuquerque and Casadevall, ; Franceschetti et al.

However, in the case of Cryptococcus neoformansa human basidiomycete pathogen, QS is regulated via secreted peptides Homer et al. As of yet, only limited supporting evidence is available concerning the roles of SSPs in communication between cells of the same organism, and between hyphae within a colony Vincent et al.

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While still scarce, these data may indicate that Ssp1 indeed could have the potential to function in cell-to-cell communication, and act as a regulator after initiation of al transduction in a dose-dependent manner for a proposed model, see Figure 1. Figure 1.

Seeking the roles for fungal small-secreted proteins in affecting saprophytic lifestyles

Scheme representing the speculated model for developmental regulation by Ssp1 in P. Ssp1 is transcriptionally upregulated after the fungus is either exposed to chemical cues such as HMF or aryl-alcohols or reaching the end of the trophophase. After the cleavage of the al peptide, they are secreted to the medium. Then, they interact with a yet to be identified transporter to initiate a al cascade, which in the onset of idiophase accompanied by secondary metabolism, generation of yellow pigment and aging.

Dashed arrows and shapes represent pathways that are yet to be found. Another intriguing possibility arises from recent evidence on the ability of some saprophytes to exhibit facultative biotrophic attributes.

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In fact, 34 out of species of wood-decay basidiomycetes were shown to be able to colonize the roots of at least one tree species, supporting the feasibility for facultative biotrophic relationships in some free-living saprotrophs Smith et al. Research on the genus Amanita showed that the origin of the genetic toolkit required for symbiosis is found in a saprotrophic species Hess et al.

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They are characteristically shorter than amino acids in length and have a al peptide.