Limits...
A eukaryotic-acquired gene by a biotrophic phytopathogen allows prolonged survival on the host by counteracting the shut-down of plant photosynthesis.

Garavaglia BS, Thomas L, Gottig N, Dunger G, Garofalo CG, Daurelio LD, Ndimba B, Orellano EG, Gehring C, Ottado J - PLoS ONE (2010)

Bottom Line: However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen.The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses.We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biology Division, Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.

ABSTRACT
Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.

Show MeSH

Related in: MedlinePlus

Model of XacPNP action in citrus canker.Typical citrus leaves lesions with ΔXacPNP (left) and Xcc wild type (right) are observed in the bottom images where differences in tissue necrosis are shown. On the leaf is a proposed model for PNP-dependent cellular processes (described in the text). Solid arrows indicate experimentally confirmed functions and dashed arrows indicate proposed mechanisms.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2812515&req=5

pone-0008950-g005: Model of XacPNP action in citrus canker.Typical citrus leaves lesions with ΔXacPNP (left) and Xcc wild type (right) are observed in the bottom images where differences in tissue necrosis are shown. On the leaf is a proposed model for PNP-dependent cellular processes (described in the text). Solid arrows indicate experimentally confirmed functions and dashed arrows indicate proposed mechanisms.

Mentions: The relationship between photosynthesis and its particular role in energy generation for the defense program has been a matter of controversy. Although it is rational to consider that energy and carbon skeletons required for plant defense has to be sustained by increases in photosynthesis, several studies demonstrate that this is not the case (reviewed in [11]). It has been proposed that a priority in infected plants is the production of defense-related compounds and that the disposable cellular activities such as the primary metabolism may be reduced [11]. In fact, many reports on photosynthesis and plant defense have shown that rates of photosynthesis are reduced after treatment with virulent or avirulent pathogens with the main difference being the timing of this reduction [12], [38]–[40]. X. citri pv. citri is a Gram-negative bacterial pathogen that uses the type III protein secretion system to translocate effector proteins into the host cell [2]. These effectors suppress basal defense responses and collectively contribute to the disease. Many effector proteins are believed to be localized in the host cell cytoplasm or in the nucleus [41]. In spite of the vast number of pathogen effector proteins identified to-date the P. syringae effector HopI1 is the only one that seems targeted to the chloroplast where it induces remodeling of the thylakoid structure [42]. Chloroplast function can also be altered by the fungal virulence protein, ToxA produced by the wheat pathogen Pyrenophora triticirepentis that interacts with a plastid protein necessary for thylakoid membrane organization [43]. We propose that Xcc has acquired and adapted a plant protein and mimics its function to maintain host conditions better suited to its biotrophic lifestyle and doing so by directly or indirectly modulating and/or sustaining chloroplast function. Accordingly, we suggest a model in which XacPNP produced by X. citri pv. citri mimics host PNP functions. These include the increase of cGMP either directly through receptor like guanylyl cyclase (particulate GCs) or indirectly through the activation of soluble guanylyl cylases (sGCs). Among the effects produced by PNP and/or cGMP-dependent signalling are the regulation of plant cell homeostasis and water uptake by modification of ion channels, activation of kinases and transcription, and the regulation of chloroplast function. Consequently, XacPNP enables more efficient photosynthesis resulting in a delay in tissue necrosis to the benefit of the biotrophic pathogen (Figure 5).


A eukaryotic-acquired gene by a biotrophic phytopathogen allows prolonged survival on the host by counteracting the shut-down of plant photosynthesis.

Garavaglia BS, Thomas L, Gottig N, Dunger G, Garofalo CG, Daurelio LD, Ndimba B, Orellano EG, Gehring C, Ottado J - PLoS ONE (2010)

Model of XacPNP action in citrus canker.Typical citrus leaves lesions with ΔXacPNP (left) and Xcc wild type (right) are observed in the bottom images where differences in tissue necrosis are shown. On the leaf is a proposed model for PNP-dependent cellular processes (described in the text). Solid arrows indicate experimentally confirmed functions and dashed arrows indicate proposed mechanisms.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2812515&req=5

pone-0008950-g005: Model of XacPNP action in citrus canker.Typical citrus leaves lesions with ΔXacPNP (left) and Xcc wild type (right) are observed in the bottom images where differences in tissue necrosis are shown. On the leaf is a proposed model for PNP-dependent cellular processes (described in the text). Solid arrows indicate experimentally confirmed functions and dashed arrows indicate proposed mechanisms.
Mentions: The relationship between photosynthesis and its particular role in energy generation for the defense program has been a matter of controversy. Although it is rational to consider that energy and carbon skeletons required for plant defense has to be sustained by increases in photosynthesis, several studies demonstrate that this is not the case (reviewed in [11]). It has been proposed that a priority in infected plants is the production of defense-related compounds and that the disposable cellular activities such as the primary metabolism may be reduced [11]. In fact, many reports on photosynthesis and plant defense have shown that rates of photosynthesis are reduced after treatment with virulent or avirulent pathogens with the main difference being the timing of this reduction [12], [38]–[40]. X. citri pv. citri is a Gram-negative bacterial pathogen that uses the type III protein secretion system to translocate effector proteins into the host cell [2]. These effectors suppress basal defense responses and collectively contribute to the disease. Many effector proteins are believed to be localized in the host cell cytoplasm or in the nucleus [41]. In spite of the vast number of pathogen effector proteins identified to-date the P. syringae effector HopI1 is the only one that seems targeted to the chloroplast where it induces remodeling of the thylakoid structure [42]. Chloroplast function can also be altered by the fungal virulence protein, ToxA produced by the wheat pathogen Pyrenophora triticirepentis that interacts with a plastid protein necessary for thylakoid membrane organization [43]. We propose that Xcc has acquired and adapted a plant protein and mimics its function to maintain host conditions better suited to its biotrophic lifestyle and doing so by directly or indirectly modulating and/or sustaining chloroplast function. Accordingly, we suggest a model in which XacPNP produced by X. citri pv. citri mimics host PNP functions. These include the increase of cGMP either directly through receptor like guanylyl cyclase (particulate GCs) or indirectly through the activation of soluble guanylyl cylases (sGCs). Among the effects produced by PNP and/or cGMP-dependent signalling are the regulation of plant cell homeostasis and water uptake by modification of ion channels, activation of kinases and transcription, and the regulation of chloroplast function. Consequently, XacPNP enables more efficient photosynthesis resulting in a delay in tissue necrosis to the benefit of the biotrophic pathogen (Figure 5).

Bottom Line: However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen.The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses.We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.

View Article: PubMed Central - PubMed

Affiliation: Molecular Biology Division, Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.

ABSTRACT
Xanthomonas citri pv. citri, the bacteria responsible for citrus canker posses a biological active plant natriuretic peptide (PNP)-like protein, not present in any other bacteria. PNPs are a class of extracellular, systemically mobile peptides that elicit a number of plant responses important in homeostasis and growth. Previously, we showed that a Xanthomonas citri pv. citri mutant lacking the PNP-like protein XacPNP produced more necrotic lesions in citrus leaves than wild type infections and suggested a role for XacPNP in the regulation of host homeostasis. Here we have analyzed the proteome modifications observed in citrus leaves infected with the wild type and XacPNP deletion mutant bacteria. While both of them cause down-regulation of enzymes related to photosynthesis as well as chloroplastic ribosomal proteins, proteins related to defense responses are up-regulated. However, leaves infiltrated with the XacPNP deletion mutant show a more pronounced decrease in photosynthetic proteins while no reduction in defense related proteins as compared to the wild-type pathogen. This suggests that XacPNP serves the pathogen to maintain host photosynthetic efficiency during pathogenesis. The results from the proteomics analyses are consistent with our chlorophyll fluorescence data and transcript analyses of defense genes that show a more marked reduction in photosynthesis in the mutant but no difference in the induction of genes diagnostic for biotic-stress responses. We therefore conclude that XacPNP counteracts the shut-down of host photosynthesis during infection and in that way maintains the tissue in better conditions, suggesting that the pathogen has adapted a host gene to modify its natural host and render it a better reservoir for prolonged bacterial survival and thus for further colonization.

Show MeSH
Related in: MedlinePlus