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Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response.

Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M - Front Microbiol (2016)

Bottom Line: Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI.Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death.These differences are discussed in the frame of a multilayered response to non self in fungi.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et Génétique Cellulaire, UMR 5095, Centre National de la Recherche Scientifique et Université de Bordeaux Bordeaux, France.

ABSTRACT
Recognition and response to non self is essential to development and survival of all organisms. It can occur between individuals of the same species or between different organisms. Fungi are established models for conspecific non self recognition in the form of vegetative incompatibility (VI), a genetically controlled process initiating a programmed cell death (PCD) leading to the rejection of a fusion cell between genetically different isolates of the same species. In Podospora anserina VI is controlled by members of the hnwd gene family encoding for proteins analogous to NOD Like Receptors (NLR) immune receptors in eukaryotes. It was hypothesized that the hnwd controlled VI reaction was derived from the fungal innate immune response. Here we analyze the P. anserina transcriptional responses to two bacterial species, Serratia fonticola to which P. anserina survives and S. marcescens to which P. anserina succumbs, and compare these to the transcriptional response induced under VI conditions. Transcriptional responses to both bacteria largely overlap, however the number of genes regulated and magnitude of regulation is more important when P. anserina survives. Transcriptional responses to bacteria also overlap with the VI reaction for both up or down regulated gene sets. Genes up regulated tend to be clustered in the genome, and display limited phylogenetic distribution. In all three responses we observed genes related to autophagy to be up-regulated. Autophagy contributes to the fungal survival in all three conditions. Genes encoding for secondary metabolites and histidine kinase signaling are also up regulated in all three conditions. Transcriptional responses also display differences. Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI. Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death. These differences are discussed in the frame of a multilayered response to non self in fungi.

No MeSH data available.


Related in: MedlinePlus

Overview of the biological functions regulated in response to non self. Biological functions or pathways significantly enriched in up (red) or down (green) regulated gene sets in response to different non self signals are represented. Functions differentially regulated by the same non self signals are grouped in colored boxes, arrows indicating the inducing conditions.
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Figure 9: Overview of the biological functions regulated in response to non self. Biological functions or pathways significantly enriched in up (red) or down (green) regulated gene sets in response to different non self signals are represented. Functions differentially regulated by the same non self signals are grouped in colored boxes, arrows indicating the inducing conditions.

Mentions: From Pfam-A or GO annotations we identified biological functions up or down regulated in response to non self that are summed up in Figure 9. All three conditions result in a growth arrest that is reflected by functions encoded by the down regulated genes mostly related to protein synthesis and growth. The conserved up regulated functions common to all three conditions are common in responses to stress (HK signaling, autophagy) and biotic interactions (autophagy and secondary metabolites). Interestingly, all functions specifically up regulated in response to one or both bacteria (SSPs, response to oxidative stress and light response, and response to fungicide through HK signaling, MFS transporters, vacuolar pH regulation) could promote fungal cell survival. For instance, P. anserina expresses more transcription factors and MFS transporters and survives better in response to S. fonticola than in response to S. marcescens, and difference in gene expression and survival may be dependent on the arsenal of bacterial pathogenicity effecters they produce (Guichard et al., 2014). In contrast, most functions specifically up regulated in the VI reaction seem to promote fungal cell death. The HET domain is an activator of a VI-like cell death (Paoletti and Clavé, 2007), HeLo and HeLo like domains act as pore forming toxins (Daskalov et al., 2015). Except for a few NLR controlling VI (Saupe et al., 1995; Espagne et al., 2002; Choi et al., 2011) fungal NLR functions have not been characterized but they often display HET or HeLo N-terminal effector domains. LysM domain function has not been defined in fungi, but it is known to bind sugars and promote immune responses in plants (Miya et al., 2007; Gimenez-Ibanez et al., 2009; Tanaka et al., 2013; Akcapinar et al., 2015). From these observations, one might propose that like plants and animals, fungi are endowed with a multilayered innate immune system that can be sequentially activated depending on the signals detected. Detection of conserved bacterial PAMPs from long range may initiate a robust and fairly conserved response whose aim is to promote fungal survival while making life of the pathogen difficult. Indeed most fungi will encounter all sorts of bacteria during their life time which will require a global response to keep them at bay. This would be comparable to the plant PTI (Jones and Dangl, 2006). Then, adapted bacteria may be able to subdue this first line of defense through the action of specifically evolved effectors. Detection of the resulting danger signals would then initiate the ultimate fungal response by triggering a localized cell death reaction through NLR signaling to restrict further invasion of the entire mycelium in a response similar to the plant Hypersensitive Response (Jones and Dangl, 2006). Positive feedback on NLR encoding genes, and standalone N-terminal effecter genes, could ensure robustness of the response by initiating multiple death pathways thereby preventing pathogens from developing inhibitors of a single pathway.


Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response.

Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M - Front Microbiol (2016)

Overview of the biological functions regulated in response to non self. Biological functions or pathways significantly enriched in up (red) or down (green) regulated gene sets in response to different non self signals are represented. Functions differentially regulated by the same non self signals are grouped in colored boxes, arrows indicating the inducing conditions.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835503&req=5

Figure 9: Overview of the biological functions regulated in response to non self. Biological functions or pathways significantly enriched in up (red) or down (green) regulated gene sets in response to different non self signals are represented. Functions differentially regulated by the same non self signals are grouped in colored boxes, arrows indicating the inducing conditions.
Mentions: From Pfam-A or GO annotations we identified biological functions up or down regulated in response to non self that are summed up in Figure 9. All three conditions result in a growth arrest that is reflected by functions encoded by the down regulated genes mostly related to protein synthesis and growth. The conserved up regulated functions common to all three conditions are common in responses to stress (HK signaling, autophagy) and biotic interactions (autophagy and secondary metabolites). Interestingly, all functions specifically up regulated in response to one or both bacteria (SSPs, response to oxidative stress and light response, and response to fungicide through HK signaling, MFS transporters, vacuolar pH regulation) could promote fungal cell survival. For instance, P. anserina expresses more transcription factors and MFS transporters and survives better in response to S. fonticola than in response to S. marcescens, and difference in gene expression and survival may be dependent on the arsenal of bacterial pathogenicity effecters they produce (Guichard et al., 2014). In contrast, most functions specifically up regulated in the VI reaction seem to promote fungal cell death. The HET domain is an activator of a VI-like cell death (Paoletti and Clavé, 2007), HeLo and HeLo like domains act as pore forming toxins (Daskalov et al., 2015). Except for a few NLR controlling VI (Saupe et al., 1995; Espagne et al., 2002; Choi et al., 2011) fungal NLR functions have not been characterized but they often display HET or HeLo N-terminal effector domains. LysM domain function has not been defined in fungi, but it is known to bind sugars and promote immune responses in plants (Miya et al., 2007; Gimenez-Ibanez et al., 2009; Tanaka et al., 2013; Akcapinar et al., 2015). From these observations, one might propose that like plants and animals, fungi are endowed with a multilayered innate immune system that can be sequentially activated depending on the signals detected. Detection of conserved bacterial PAMPs from long range may initiate a robust and fairly conserved response whose aim is to promote fungal survival while making life of the pathogen difficult. Indeed most fungi will encounter all sorts of bacteria during their life time which will require a global response to keep them at bay. This would be comparable to the plant PTI (Jones and Dangl, 2006). Then, adapted bacteria may be able to subdue this first line of defense through the action of specifically evolved effectors. Detection of the resulting danger signals would then initiate the ultimate fungal response by triggering a localized cell death reaction through NLR signaling to restrict further invasion of the entire mycelium in a response similar to the plant Hypersensitive Response (Jones and Dangl, 2006). Positive feedback on NLR encoding genes, and standalone N-terminal effecter genes, could ensure robustness of the response by initiating multiple death pathways thereby preventing pathogens from developing inhibitors of a single pathway.

Bottom Line: Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI.Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death.These differences are discussed in the frame of a multilayered response to non self in fungi.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et Génétique Cellulaire, UMR 5095, Centre National de la Recherche Scientifique et Université de Bordeaux Bordeaux, France.

ABSTRACT
Recognition and response to non self is essential to development and survival of all organisms. It can occur between individuals of the same species or between different organisms. Fungi are established models for conspecific non self recognition in the form of vegetative incompatibility (VI), a genetically controlled process initiating a programmed cell death (PCD) leading to the rejection of a fusion cell between genetically different isolates of the same species. In Podospora anserina VI is controlled by members of the hnwd gene family encoding for proteins analogous to NOD Like Receptors (NLR) immune receptors in eukaryotes. It was hypothesized that the hnwd controlled VI reaction was derived from the fungal innate immune response. Here we analyze the P. anserina transcriptional responses to two bacterial species, Serratia fonticola to which P. anserina survives and S. marcescens to which P. anserina succumbs, and compare these to the transcriptional response induced under VI conditions. Transcriptional responses to both bacteria largely overlap, however the number of genes regulated and magnitude of regulation is more important when P. anserina survives. Transcriptional responses to bacteria also overlap with the VI reaction for both up or down regulated gene sets. Genes up regulated tend to be clustered in the genome, and display limited phylogenetic distribution. In all three responses we observed genes related to autophagy to be up-regulated. Autophagy contributes to the fungal survival in all three conditions. Genes encoding for secondary metabolites and histidine kinase signaling are also up regulated in all three conditions. Transcriptional responses also display differences. Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI. Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death. These differences are discussed in the frame of a multilayered response to non self in fungi.

No MeSH data available.


Related in: MedlinePlus