Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction
Abstract Background Fungal pathogens like Fusarium graminearum can cause severe yield losses and mycotoxin contamination of food and feed worldwide. We recently showed its ability to systemically colonize wheat via root infection. However, the molecular response of wheat to Fusarium root rot (FRR) i...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-11-01
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| Series: | Plant Methods |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13007-018-0368-6 |
| _version_ | 1818163257467207680 |
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| author | Dhaka Ram Bhandari Qing Wang Bin Li Wolfgang Friedt Andreas Römpp Bernhard Spengler Sven Gottwald |
| author_facet | Dhaka Ram Bhandari Qing Wang Bin Li Wolfgang Friedt Andreas Römpp Bernhard Spengler Sven Gottwald |
| author_sort | Dhaka Ram Bhandari |
| collection | DOAJ |
| description | Abstract Background Fungal pathogens like Fusarium graminearum can cause severe yield losses and mycotoxin contamination of food and feed worldwide. We recently showed its ability to systemically colonize wheat via root infection. However, the molecular response of wheat to Fusarium root rot (FRR) infection and systemic spread is still unknown. As a molecular camera, mass spectrometry (MS) imaging combines label-free and multiplex metabolite profiling with histopathology. Results Atmospheric-pressure (AP)-SMALDI-MS imaging was combined with optical microscopy to study wheat-F. graminearum interaction at the root–shoot junction, which is a crucial line of defense against a pathogen that can invade all distal plant parts. To scope the functional, temporal and local aspects of FRR disease spread, metabolic changes were simultaneous visualized in diseased and healthy stem bases of the resistant cultivar Florence-Aurore at 10, 14 and 21 days after root inoculation. Histological information was used to identify disease relevant tissues and to assist the interpretation of molecular images. Detected mycotoxin compounds secreted by F. graminearum showed a route of stem infection that was consistent with observations made by microscopy. The outer epidermis and vasculature of leaf sheath were, at different disease stages, identified as prominent sites of pathogen migration and wheat protection. Wheat metabolites mapped to these relatively small tissues indicated cell wall strengthening and antifungal activity as direct defenses as well as conservation in the wheat reactions to F. graminearum diseases that affect different plant organs. Conclusions AP-SMALDI-MS imaging at high spatial resolution is a versatile technique that can be applied to basic and applied aspects of agricultural research. Combining the technology with optical microscopy was found to be a powerful tool to gain in-depth information on almost unknown crop disease. Moreover, the approach allowed studying metabolism at the host–pathogen interface. The results provide important hints to an understanding of the complex spatio-temporal organization of plant resistance. Defense-on-demand responses to pathogen ingress were found, which provide opportunities for future research towards an improved resistance that does not negatively impact yield development in the field by saving plant resources and, moreover, may control different Fusarium diseases. |
| first_indexed | 2024-12-11T16:46:41Z |
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| id | doaj.art-dbbbe7c073df4765835f379d9b40b45b |
| institution | Directory Open Access Journal |
| issn | 1746-4811 |
| language | English |
| last_indexed | 2024-12-11T16:46:41Z |
| publishDate | 2018-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Plant Methods |
| spelling | doaj.art-dbbbe7c073df4765835f379d9b40b45b2022-12-22T00:58:11ZengBMCPlant Methods1746-48112018-11-0114111310.1186/s13007-018-0368-6Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junctionDhaka Ram Bhandari0Qing Wang1Bin Li2Wolfgang Friedt3Andreas Römpp4Bernhard Spengler5Sven Gottwald6Institute of Inorganic and Analytical Chemistry, Justus Liebig University GiessenDepartment of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig UniversityState Key Laboratory of Natural Medicines, China Pharmaceutical UniversityDepartment of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig UniversityChair of Bioanalytical Sciences and Food Analysis, University of BayreuthInstitute of Inorganic and Analytical Chemistry, Justus Liebig University GiessenInstitute of Inorganic and Analytical Chemistry, Justus Liebig University GiessenAbstract Background Fungal pathogens like Fusarium graminearum can cause severe yield losses and mycotoxin contamination of food and feed worldwide. We recently showed its ability to systemically colonize wheat via root infection. However, the molecular response of wheat to Fusarium root rot (FRR) infection and systemic spread is still unknown. As a molecular camera, mass spectrometry (MS) imaging combines label-free and multiplex metabolite profiling with histopathology. Results Atmospheric-pressure (AP)-SMALDI-MS imaging was combined with optical microscopy to study wheat-F. graminearum interaction at the root–shoot junction, which is a crucial line of defense against a pathogen that can invade all distal plant parts. To scope the functional, temporal and local aspects of FRR disease spread, metabolic changes were simultaneous visualized in diseased and healthy stem bases of the resistant cultivar Florence-Aurore at 10, 14 and 21 days after root inoculation. Histological information was used to identify disease relevant tissues and to assist the interpretation of molecular images. Detected mycotoxin compounds secreted by F. graminearum showed a route of stem infection that was consistent with observations made by microscopy. The outer epidermis and vasculature of leaf sheath were, at different disease stages, identified as prominent sites of pathogen migration and wheat protection. Wheat metabolites mapped to these relatively small tissues indicated cell wall strengthening and antifungal activity as direct defenses as well as conservation in the wheat reactions to F. graminearum diseases that affect different plant organs. Conclusions AP-SMALDI-MS imaging at high spatial resolution is a versatile technique that can be applied to basic and applied aspects of agricultural research. Combining the technology with optical microscopy was found to be a powerful tool to gain in-depth information on almost unknown crop disease. Moreover, the approach allowed studying metabolism at the host–pathogen interface. The results provide important hints to an understanding of the complex spatio-temporal organization of plant resistance. Defense-on-demand responses to pathogen ingress were found, which provide opportunities for future research towards an improved resistance that does not negatively impact yield development in the field by saving plant resources and, moreover, may control different Fusarium diseases.http://link.springer.com/article/10.1186/s13007-018-0368-6Mass spectrometry-based histopathologyAP-SMALDI-MS imagingConfocal laser scanning microscopyFusarium graminearumFusarium root rotWheat |
| spellingShingle | Dhaka Ram Bhandari Qing Wang Bin Li Wolfgang Friedt Andreas Römpp Bernhard Spengler Sven Gottwald Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction Plant Methods Mass spectrometry-based histopathology AP-SMALDI-MS imaging Confocal laser scanning microscopy Fusarium graminearum Fusarium root rot Wheat |
| title | Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction |
| title_full | Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction |
| title_fullStr | Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction |
| title_full_unstemmed | Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction |
| title_short | Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction |
| title_sort | histology guided high resolution ap smaldi mass spectrometry imaging of wheat fusarium graminearum interaction at the root shoot junction |
| topic | Mass spectrometry-based histopathology AP-SMALDI-MS imaging Confocal laser scanning microscopy Fusarium graminearum Fusarium root rot Wheat |
| url | http://link.springer.com/article/10.1186/s13007-018-0368-6 |
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