Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity
Septoria nodorum blotch is a major disease of wheat caused by the fungus Parastagonospora nodorum. Recent studies have demonstrated that secondary metabolites, including polyketides and non-ribosomal peptides, produced by the pathogen play important roles in disease and development. However, there i...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00466/full |
| _version_ | 1818021217538408448 |
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| author | Mariano Jordi Muria-Gonzalez Yeannie Yeng Yeannie Yeng Susan Breen Oliver Mead Chen Wang Yi-Heng Chooi Russell A. Barrow Russell A. Barrow Peter S. Solomon |
| author_facet | Mariano Jordi Muria-Gonzalez Yeannie Yeng Yeannie Yeng Susan Breen Oliver Mead Chen Wang Yi-Heng Chooi Russell A. Barrow Russell A. Barrow Peter S. Solomon |
| author_sort | Mariano Jordi Muria-Gonzalez |
| collection | DOAJ |
| description | Septoria nodorum blotch is a major disease of wheat caused by the fungus Parastagonospora nodorum. Recent studies have demonstrated that secondary metabolites, including polyketides and non-ribosomal peptides, produced by the pathogen play important roles in disease and development. However, there is currently no knowledge on the composition or biological activity of the volatile organic compounds (VOCs) secreted by P. nodorum. To address this, we undertook a series of growth and phytotoxicity assays and demonstrated that P. nodorum VOCs inhibited bacterial growth, were phytotoxic and suppressed self-growth. Mass spectrometry analysis revealed that 3-methyl-1-butanol, 2-methyl-1-butanol, 2-methyl-1-propanol, and 2-phenylethanol were dominant in the VOC mixture and phenotypic assays using these short chain alcohols confirmed that they were phytotoxic. Further analysis of the VOCs also identified the presence of multiple sesquiterpenes of which four were identified via mass spectrometry and nuclear magnetic resonance as β-elemene, α-cyperone, eudesma-4,11-diene and acora-4,9-diene. Subsequent reverse genetics studies were able to link these molecules to corresponding sesquiterpene synthases in the P. nodorum genome. However, despite extensive testing, these molecules were not involved in either of the growth inhibition or phytotoxicity phenotypes previously observed. Plant assays using mutants of the pathogen lacking the synthetic genes revealed that the identified sesquiterpenes were not required for disease formation on wheat leaves. Collectively, these data have significantly extended our knowledge of the VOCs in fungi and provided the basis for further dissecting the roles of sesquiterpenes in plant disease. |
| first_indexed | 2024-04-14T08:15:48Z |
| format | Article |
| id | doaj.art-af66d7fd73da48dbb8f95ec73ff4749f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-14T08:15:48Z |
| publishDate | 2020-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-af66d7fd73da48dbb8f95ec73ff4749f2022-12-22T02:04:25ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-03-011110.3389/fmicb.2020.00466507043Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and PhytotoxicityMariano Jordi Muria-Gonzalez0Yeannie Yeng1Yeannie Yeng2Susan Breen3Oliver Mead4Chen Wang5Yi-Heng Chooi6Russell A. Barrow7Russell A. Barrow8Peter S. Solomon9Research School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaResearch School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaDepartment of Oral Biology and Biomedical Sciences, MAHSA University, Selangor, MalaysiaResearch School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaResearch School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaResearch School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaSchool of Molecular Sciences, University of Western Australia, Perth, WA, AustraliaGraham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, NSW, AustraliaPlus 3 Australia Pty Ltd., Hawker, ACT, AustraliaResearch School of Biology, ACT, Australian National University, Canberra, ACT, AustraliaSeptoria nodorum blotch is a major disease of wheat caused by the fungus Parastagonospora nodorum. Recent studies have demonstrated that secondary metabolites, including polyketides and non-ribosomal peptides, produced by the pathogen play important roles in disease and development. However, there is currently no knowledge on the composition or biological activity of the volatile organic compounds (VOCs) secreted by P. nodorum. To address this, we undertook a series of growth and phytotoxicity assays and demonstrated that P. nodorum VOCs inhibited bacterial growth, were phytotoxic and suppressed self-growth. Mass spectrometry analysis revealed that 3-methyl-1-butanol, 2-methyl-1-butanol, 2-methyl-1-propanol, and 2-phenylethanol were dominant in the VOC mixture and phenotypic assays using these short chain alcohols confirmed that they were phytotoxic. Further analysis of the VOCs also identified the presence of multiple sesquiterpenes of which four were identified via mass spectrometry and nuclear magnetic resonance as β-elemene, α-cyperone, eudesma-4,11-diene and acora-4,9-diene. Subsequent reverse genetics studies were able to link these molecules to corresponding sesquiterpene synthases in the P. nodorum genome. However, despite extensive testing, these molecules were not involved in either of the growth inhibition or phytotoxicity phenotypes previously observed. Plant assays using mutants of the pathogen lacking the synthetic genes revealed that the identified sesquiterpenes were not required for disease formation on wheat leaves. Collectively, these data have significantly extended our knowledge of the VOCs in fungi and provided the basis for further dissecting the roles of sesquiterpenes in plant disease.https://www.frontiersin.org/article/10.3389/fmicb.2020.00466/fullwheat pathogensvolatilesdiseasesesquiterpenesParastagonosopora nodorum |
| spellingShingle | Mariano Jordi Muria-Gonzalez Yeannie Yeng Yeannie Yeng Susan Breen Oliver Mead Chen Wang Yi-Heng Chooi Russell A. Barrow Russell A. Barrow Peter S. Solomon Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity Frontiers in Microbiology wheat pathogens volatiles disease sesquiterpenes Parastagonosopora nodorum |
| title | Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity |
| title_full | Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity |
| title_fullStr | Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity |
| title_full_unstemmed | Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity |
| title_short | Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity |
| title_sort | volatile molecules secreted by the wheat pathogen parastagonospora nodorum are involved in development and phytotoxicity |
| topic | wheat pathogens volatiles disease sesquiterpenes Parastagonosopora nodorum |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00466/full |
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