Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria
Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to lim...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-07-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2017.01158/full |
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| author | Juan J. Pierella Karlusich Matias D. Zurbriggen Fahimeh Shahinnia Sophia Sonnewald Uwe Sonnewald Seyed A. Hosseini Mohammad-Reza Hajirezaei Néstor Carrillo |
| author_facet | Juan J. Pierella Karlusich Matias D. Zurbriggen Fahimeh Shahinnia Sophia Sonnewald Uwe Sonnewald Seyed A. Hosseini Mohammad-Reza Hajirezaei Néstor Carrillo |
| author_sort | Juan J. Pierella Karlusich |
| collection | DOAJ |
| description | Non-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses. |
| first_indexed | 2024-12-12T15:17:58Z |
| format | Article |
| id | doaj.art-7809ecaee3fa4ecea9826d475fe32cf2 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-12T15:17:58Z |
| publishDate | 2017-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-7809ecaee3fa4ecea9826d475fe32cf22022-12-22T00:20:27ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-07-01810.3389/fpls.2017.01158251518Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoriaJuan J. Pierella Karlusich0Matias D. Zurbriggen1Fahimeh Shahinnia2Sophia Sonnewald3Uwe Sonnewald4Seyed A. Hosseini5Mohammad-Reza Hajirezaei6Néstor Carrillo7Instituto de Biología Molecular y Celular de Rosario (Consejo Nacional de Investigaciones Científicas y Técnicas), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de RosarioRosario, ArgentinaInstituto de Biología Molecular y Celular de Rosario (Consejo Nacional de Investigaciones Científicas y Técnicas), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de RosarioRosario, ArgentinaLeibniz Institute of Plant Genetics and Crop Plant ResearchGatersleben, GermanyDepartment of Biology, Division of Biochemistry, Friedrich-Alexander-University Erlangen-NurembergErlangen, GermanyDepartment of Biology, Division of Biochemistry, Friedrich-Alexander-University Erlangen-NurembergErlangen, GermanyLeibniz Institute of Plant Genetics and Crop Plant ResearchGatersleben, GermanyLeibniz Institute of Plant Genetics and Crop Plant ResearchGatersleben, GermanyInstituto de Biología Molecular y Celular de Rosario (Consejo Nacional de Investigaciones Científicas y Técnicas), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de RosarioRosario, ArgentinaNon-host resistance is the most ample and durable form of plant resistance against pathogen infection. It includes induction of defense-associated genes, massive metabolic reprogramming, and in many instances, a form of localized cell death (LCD) at the site of infection, purportedly designed to limit the spread of biotrophic and hemibiotrophic microorganisms. Reactive oxygen species (ROS) have been proposed to act as signals for LCD orchestration. They are produced in various cellular compartments including chloroplasts, mitochondria and apoplast. We have previously reported that down-regulation of ROS build-up in chloroplasts by expression of a plastid-targeted flavodoxin (Fld) suppressed LCD in tobacco leaves inoculated with the non-host bacterium Xanthomonas campestris pv. vesicatoria (Xcv), while other defensive responses were unaffected, suggesting that chloroplast ROS and/or redox status play a major role in the progress of LCD. To better understand these effects, we compare here the transcriptomic alterations caused by Xcv inoculation on leaves of Fld-expressing tobacco plants and their wild-type siblings. About 29% of leaf-expressed genes were affected by Xcv and/or Fld. Surprisingly, 5.8% of them (1,111 genes) were regulated by Fld in the absence of infection, presumably representing pathways responsive to chloroplast ROS production and/or redox status during normal growth conditions. While the majority (∼75%) of pathogen-responsive genes were not affected by Fld, many Xcv responses were exacerbated, attenuated, or regulated in opposite direction by expression of this protein. Particularly interesting was a group of 384 genes displaying Xcv responses that were already triggered by Fld in the absence of infection, suggesting that the transgenic plants had a larger and more diversified suite of constitutive defenses against the attacking microorganism compared to the wild type. Fld modulated many genes involved in pathogenesis, signal transduction, transcriptional regulation and hormone-based pathways. Remarkable interactions with proteasomal protein degradation were observed. The results provide the first genome-wide, comprehensive picture illustrating the relevance of chloroplast redox status in biotic stress responses.http://journal.frontiersin.org/article/10.3389/fpls.2017.01158/fullplant-microbe interactionschloroplast redox statusreactive oxygen speciestranscriptomicsflavodoxinlocalized cell death |
| spellingShingle | Juan J. Pierella Karlusich Matias D. Zurbriggen Fahimeh Shahinnia Sophia Sonnewald Uwe Sonnewald Seyed A. Hosseini Mohammad-Reza Hajirezaei Néstor Carrillo Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria Frontiers in Plant Science plant-microbe interactions chloroplast redox status reactive oxygen species transcriptomics flavodoxin localized cell death |
| title | Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria |
| title_full | Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria |
| title_fullStr | Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria |
| title_full_unstemmed | Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria |
| title_short | Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria |
| title_sort | chloroplast redox status modulates genome wide plant responses during the non host interaction of tobacco with the hemibiotrophic bacterium xanthomonas campestris pv vesicatoria |
| topic | plant-microbe interactions chloroplast redox status reactive oxygen species transcriptomics flavodoxin localized cell death |
| url | http://journal.frontiersin.org/article/10.3389/fpls.2017.01158/full |
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