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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

Comparison of the differentially expressed genes in response to bacteria. (A,B) Venn diagram showing P. anserina genes up or down regulated in response to S. fonticola or S. marcescens. (C,D) Correlation of the fold change level in response to both bacteria. For each gene expressed in both conditions, LogFc levels in response to both bacteria are reported. Genes are ordered along the X-axis according to increasing LogFc values (C) in response to S. marcescens for genes up regulated and decreasing LogFc values (D) in response to S. marcescens for genes down regulated. (E,F) Magnitude of transcriptional regulation is more important in response to S. fonticola than in response to S. marcescens. Histograms represent the number of genes that are more up (E) or down (F) regulated in response to S. fonticola or S. marcescens in the VsSf or VsSm data sets, at each time point, or for different LogFc values. Fisher tests were conducted to compare number the number of genes with a greater level of regulation in response to both bacteria (**p < 0.001, *p < 0.05).
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Figure 2: Comparison of the differentially expressed genes in response to bacteria. (A,B) Venn diagram showing P. anserina genes up or down regulated in response to S. fonticola or S. marcescens. (C,D) Correlation of the fold change level in response to both bacteria. For each gene expressed in both conditions, LogFc levels in response to both bacteria are reported. Genes are ordered along the X-axis according to increasing LogFc values (C) in response to S. marcescens for genes up regulated and decreasing LogFc values (D) in response to S. marcescens for genes down regulated. (E,F) Magnitude of transcriptional regulation is more important in response to S. fonticola than in response to S. marcescens. Histograms represent the number of genes that are more up (E) or down (F) regulated in response to S. fonticola or S. marcescens in the VsSf or VsSm data sets, at each time point, or for different LogFc values. Fisher tests were conducted to compare number the number of genes with a greater level of regulation in response to both bacteria (**p < 0.001, *p < 0.05).

Mentions: We first compared P. anserina transcriptional responses to both bacteria. As indicated in Figure 2, both responses largely overlap (Fisher test, p = 0), and the response to S. marcescens is almost entirely included in the response to S. fonticola. Only 12 and 9.5% of the genes up or down regulated in the VsSm set were not in the VsSf set, while 21 and 22% of the VsSf set were not in the VsSm set. This observation remains true when looking at regulated genes after 2 or 6 h of exposure to the bacteria, or when looking at expressed genes with different LogFc levels. Three hundred and ninety and 211 are up regulated specifically in response to S. fonticola or S. marcescens, while 420 and 153 genes are specifically down regulated in response to these two bacteria, respectively. When focusing on genes regulated in both conditions we observed a good correlation in the response to both bacteria (Figure 2), meaning that globally in response to both bacteria gene expression regulation follows a similar pattern. However, we observed that generally the magnitude of the differential expression, whether for up or down regulation, is more important in response to S. fonticola than in response to S. marcescens (Figure 2). In other words globally genes are more up or down regulated in response to S. fonticola than to S. marcescens. Again, this remains true for different times of exposure or when considering different logFc level.


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)

Comparison of the differentially expressed genes in response to bacteria. (A,B) Venn diagram showing P. anserina genes up or down regulated in response to S. fonticola or S. marcescens. (C,D) Correlation of the fold change level in response to both bacteria. For each gene expressed in both conditions, LogFc levels in response to both bacteria are reported. Genes are ordered along the X-axis according to increasing LogFc values (C) in response to S. marcescens for genes up regulated and decreasing LogFc values (D) in response to S. marcescens for genes down regulated. (E,F) Magnitude of transcriptional regulation is more important in response to S. fonticola than in response to S. marcescens. Histograms represent the number of genes that are more up (E) or down (F) regulated in response to S. fonticola or S. marcescens in the VsSf or VsSm data sets, at each time point, or for different LogFc values. Fisher tests were conducted to compare number the number of genes with a greater level of regulation in response to both bacteria (**p < 0.001, *p < 0.05).
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Figure 2: Comparison of the differentially expressed genes in response to bacteria. (A,B) Venn diagram showing P. anserina genes up or down regulated in response to S. fonticola or S. marcescens. (C,D) Correlation of the fold change level in response to both bacteria. For each gene expressed in both conditions, LogFc levels in response to both bacteria are reported. Genes are ordered along the X-axis according to increasing LogFc values (C) in response to S. marcescens for genes up regulated and decreasing LogFc values (D) in response to S. marcescens for genes down regulated. (E,F) Magnitude of transcriptional regulation is more important in response to S. fonticola than in response to S. marcescens. Histograms represent the number of genes that are more up (E) or down (F) regulated in response to S. fonticola or S. marcescens in the VsSf or VsSm data sets, at each time point, or for different LogFc values. Fisher tests were conducted to compare number the number of genes with a greater level of regulation in response to both bacteria (**p < 0.001, *p < 0.05).
Mentions: We first compared P. anserina transcriptional responses to both bacteria. As indicated in Figure 2, both responses largely overlap (Fisher test, p = 0), and the response to S. marcescens is almost entirely included in the response to S. fonticola. Only 12 and 9.5% of the genes up or down regulated in the VsSm set were not in the VsSf set, while 21 and 22% of the VsSf set were not in the VsSm set. This observation remains true when looking at regulated genes after 2 or 6 h of exposure to the bacteria, or when looking at expressed genes with different LogFc levels. Three hundred and ninety and 211 are up regulated specifically in response to S. fonticola or S. marcescens, while 420 and 153 genes are specifically down regulated in response to these two bacteria, respectively. When focusing on genes regulated in both conditions we observed a good correlation in the response to both bacteria (Figure 2), meaning that globally in response to both bacteria gene expression regulation follows a similar pattern. However, we observed that generally the magnitude of the differential expression, whether for up or down regulation, is more important in response to S. fonticola than in response to S. marcescens (Figure 2). In other words globally genes are more up or down regulated in response to S. fonticola than to S. marcescens. Again, this remains true for different times of exposure or when considering different logFc level.

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