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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

Versatility of differentially expressed genes. (A–C) The histograms represent the number of differentially expressed genes in response to non self for each versatility category. The left scale is relevant for number for orphan or versatile genes, the right scale for core genome genes. Fisher's tests were conducted to compare number of up and down regulated genes in each category (*p < 0.05, **p < 0.001). (D,E) Number of genes up or down regulated during VI only, in response to S. fonticola only or in both conditions. Fisher's test were conducted to compare the number of genes up or down regulated specifically in either condition (*p < 0.05, **p < 0.001). (F) Distribution of the versatility level (blue line) or up regulated genes in response to S. fonticola (Red line) or during VI (green line) along each P. anserina chromosomes. Each of the seven P. anserina chromosomes was analyzed by a sliding window analysis (window size of 100 genes). For each 100 genes window, versatility is expressed as an average value (left axis), while fraction of up regulated genes is referred to the right axis. The horizontal axis represents the chromosome. Purple bars (lettered a–s) indicate regions of high density of versatile genes; arrowheads indicate regions of high density of expression specific to a given condition (green for VsSf, red for VI).
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Figure 4: Versatility of differentially expressed genes. (A–C) The histograms represent the number of differentially expressed genes in response to non self for each versatility category. The left scale is relevant for number for orphan or versatile genes, the right scale for core genome genes. Fisher's tests were conducted to compare number of up and down regulated genes in each category (*p < 0.05, **p < 0.001). (D,E) Number of genes up or down regulated during VI only, in response to S. fonticola only or in both conditions. Fisher's test were conducted to compare the number of genes up or down regulated specifically in either condition (*p < 0.05, **p < 0.001). (F) Distribution of the versatility level (blue line) or up regulated genes in response to S. fonticola (Red line) or during VI (green line) along each P. anserina chromosomes. Each of the seven P. anserina chromosomes was analyzed by a sliding window analysis (window size of 100 genes). For each 100 genes window, versatility is expressed as an average value (left axis), while fraction of up regulated genes is referred to the right axis. The horizontal axis represents the chromosome. Purple bars (lettered a–s) indicate regions of high density of versatile genes; arrowheads indicate regions of high density of expression specific to a given condition (green for VsSf, red for VI).

Mentions: Wapinski and co-authors introduced the term versatility to describe the frequency at which genes can be gained or lost during the course of evolution, and they found that genes encoding for adaptive functions are more versatile than genes encoding for essential functions (Wapinski et al., 2007). In previous studies of VI (Hutchison et al., 2009; Bidard et al., 2013), showed that up regulated gene sets included an excess of orphan genes. We analyzed versatility of genes regulated in response to non self. We approached versatility of P. anserina annotated cds by counting the number of blastp hits (cut off e-value < 1e-5) of their predicted products at the genus level in fungal genomes. We defined the fungal core genome as the genes having an ortholog in the distantly related ascomycete S. cerevisiae (3297 genes described in Bidard et al., 2013), orphans as having a blastp hit only in P. anserina (640 genes) and ranked the remaining genes (6698 sequences) in 10 versatility bins of approximately 670 sequences according to an increasing number of hits, so that smallest numbered bins contain sequences resulting in the less blastp hits (all bin compositions are presented in Additional file 1). Genes belonging to the versatile bins or orphan categories are significantly more up than down regulated [1493 up/995 down (p = 6.2e-28) for VsSf, 1386 up/790 down (p = 0) for VsSm, 1597 up/932 down (p = 0) for VI]. In contrast the core genome is more down than up regulated [354 up/886 down (p = 0) for VsSf, 282 up/825 down (p = 0) for VsSm, 317 up/991 down (p = 0) for VI]. We then analyzed the distribution of differentially expressed genes in these categories for the three responses we analyze (Figures 4A–C). In all three responses genes belonging to orphan or versatile categories are more up than down regulated. However, repartition of differentially expressed genes in versatility bins differ between VI and response to bacteria as exemplified in the comparison between VsSf and VI gene sets (Figures 4D,E). Genes up regulated during VI are more represented in the most versatile bins, while genes up regulated in response to the bacteria are more represented in the less versatile bins. Genes expressed in both conditions are equally represented in all bins. Inversely, genes down regulated in response to bacteria are more represented in the most versatile bins. The situation is identical when comparing the reaction to S. marcescens and VI (not shown).


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)

Versatility of differentially expressed genes. (A–C) The histograms represent the number of differentially expressed genes in response to non self for each versatility category. The left scale is relevant for number for orphan or versatile genes, the right scale for core genome genes. Fisher's tests were conducted to compare number of up and down regulated genes in each category (*p < 0.05, **p < 0.001). (D,E) Number of genes up or down regulated during VI only, in response to S. fonticola only or in both conditions. Fisher's test were conducted to compare the number of genes up or down regulated specifically in either condition (*p < 0.05, **p < 0.001). (F) Distribution of the versatility level (blue line) or up regulated genes in response to S. fonticola (Red line) or during VI (green line) along each P. anserina chromosomes. Each of the seven P. anserina chromosomes was analyzed by a sliding window analysis (window size of 100 genes). For each 100 genes window, versatility is expressed as an average value (left axis), while fraction of up regulated genes is referred to the right axis. The horizontal axis represents the chromosome. Purple bars (lettered a–s) indicate regions of high density of versatile genes; arrowheads indicate regions of high density of expression specific to a given condition (green for VsSf, red for VI).
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Figure 4: Versatility of differentially expressed genes. (A–C) The histograms represent the number of differentially expressed genes in response to non self for each versatility category. The left scale is relevant for number for orphan or versatile genes, the right scale for core genome genes. Fisher's tests were conducted to compare number of up and down regulated genes in each category (*p < 0.05, **p < 0.001). (D,E) Number of genes up or down regulated during VI only, in response to S. fonticola only or in both conditions. Fisher's test were conducted to compare the number of genes up or down regulated specifically in either condition (*p < 0.05, **p < 0.001). (F) Distribution of the versatility level (blue line) or up regulated genes in response to S. fonticola (Red line) or during VI (green line) along each P. anserina chromosomes. Each of the seven P. anserina chromosomes was analyzed by a sliding window analysis (window size of 100 genes). For each 100 genes window, versatility is expressed as an average value (left axis), while fraction of up regulated genes is referred to the right axis. The horizontal axis represents the chromosome. Purple bars (lettered a–s) indicate regions of high density of versatile genes; arrowheads indicate regions of high density of expression specific to a given condition (green for VsSf, red for VI).
Mentions: Wapinski and co-authors introduced the term versatility to describe the frequency at which genes can be gained or lost during the course of evolution, and they found that genes encoding for adaptive functions are more versatile than genes encoding for essential functions (Wapinski et al., 2007). In previous studies of VI (Hutchison et al., 2009; Bidard et al., 2013), showed that up regulated gene sets included an excess of orphan genes. We analyzed versatility of genes regulated in response to non self. We approached versatility of P. anserina annotated cds by counting the number of blastp hits (cut off e-value < 1e-5) of their predicted products at the genus level in fungal genomes. We defined the fungal core genome as the genes having an ortholog in the distantly related ascomycete S. cerevisiae (3297 genes described in Bidard et al., 2013), orphans as having a blastp hit only in P. anserina (640 genes) and ranked the remaining genes (6698 sequences) in 10 versatility bins of approximately 670 sequences according to an increasing number of hits, so that smallest numbered bins contain sequences resulting in the less blastp hits (all bin compositions are presented in Additional file 1). Genes belonging to the versatile bins or orphan categories are significantly more up than down regulated [1493 up/995 down (p = 6.2e-28) for VsSf, 1386 up/790 down (p = 0) for VsSm, 1597 up/932 down (p = 0) for VI]. In contrast the core genome is more down than up regulated [354 up/886 down (p = 0) for VsSf, 282 up/825 down (p = 0) for VsSm, 317 up/991 down (p = 0) for VI]. We then analyzed the distribution of differentially expressed genes in these categories for the three responses we analyze (Figures 4A–C). In all three responses genes belonging to orphan or versatile categories are more up than down regulated. However, repartition of differentially expressed genes in versatility bins differ between VI and response to bacteria as exemplified in the comparison between VsSf and VI gene sets (Figures 4D,E). Genes up regulated during VI are more represented in the most versatile bins, while genes up regulated in response to the bacteria are more represented in the less versatile bins. Genes expressed in both conditions are equally represented in all bins. Inversely, genes down regulated in response to bacteria are more represented in the most versatile bins. The situation is identical when comparing the reaction to S. marcescens and VI (not shown).

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