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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

P. anserina is submitted to an oxidative stress in response to bacteria: Upon transfer for 2 or 6 h onto S. fonticola or S. marcescens seeded plates ROS are detected in P. anserina dead or dying cells (arrowheads) that are not detected after transfer to bacteria free plates.
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Figure 8: P. anserina is submitted to an oxidative stress in response to bacteria: Upon transfer for 2 or 6 h onto S. fonticola or S. marcescens seeded plates ROS are detected in P. anserina dead or dying cells (arrowheads) that are not detected after transfer to bacteria free plates.

Mentions: ROS are often produced in the context of host/pathogen interactions either as a defense mechanism by the host or as a debilitating factor by the pathogen (Gessler et al., 2007). We have compiled P. anserina genes encoding ROS producing enzymes or acting as antioxidant agents (Additional file 5). It is clear that in reaction to bacteria, expression of antioxidant components is stimulated, which is not the case during the VI reaction, while expression of the main ROS producing enzymes (PaNOX1-3) is not stimulated. Using a probe reactive to ROS we indeed observed their accumulation in dead or dying cells in presence of bacteria (Figure 8). These observations suggest that P. anserina is confronted to an oxidative stress generated by the presence of the bacteria. It was already observed that P. anserina accumulated peroxides in response to certain fungal species but not during VI (Silar, 2005).


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)

P. anserina is submitted to an oxidative stress in response to bacteria: Upon transfer for 2 or 6 h onto S. fonticola or S. marcescens seeded plates ROS are detected in P. anserina dead or dying cells (arrowheads) that are not detected after transfer to bacteria free plates.
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Related In: Results  -  Collection

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Figure 8: P. anserina is submitted to an oxidative stress in response to bacteria: Upon transfer for 2 or 6 h onto S. fonticola or S. marcescens seeded plates ROS are detected in P. anserina dead or dying cells (arrowheads) that are not detected after transfer to bacteria free plates.
Mentions: ROS are often produced in the context of host/pathogen interactions either as a defense mechanism by the host or as a debilitating factor by the pathogen (Gessler et al., 2007). We have compiled P. anserina genes encoding ROS producing enzymes or acting as antioxidant agents (Additional file 5). It is clear that in reaction to bacteria, expression of antioxidant components is stimulated, which is not the case during the VI reaction, while expression of the main ROS producing enzymes (PaNOX1-3) is not stimulated. Using a probe reactive to ROS we indeed observed their accumulation in dead or dying cells in presence of bacteria (Figure 8). These observations suggest that P. anserina is confronted to an oxidative stress generated by the presence of the bacteria. It was already observed that P. anserina accumulated peroxides in response to certain fungal species but not during VI (Silar, 2005).

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