Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis
Fungal pathogens deploy a set of molecules (proteins, specialized metabolites, and sRNAs), so-called effectors, to aid the infection process. In comparison to other plant pathogens, smut fungi have small genomes and secretomes of 20 Mb and around 500 proteins, respectively. Previous comparative geno...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2024-03-01
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| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0139-FI |
| _version_ | 1827293033474818048 |
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| author | Mariana Schuster Gabriel Schweizer Stefanie Reißmann Petra Happel Daniela Aßmann Nicole Rössel Ulrich Güldener Gertrud Mannhaupt Nicole Ludwig Sarah Winterberg Clément Pellegrin Shigeyuki Tanaka Volker Vincon Libera Lo Presti Lei Wang Lena Bender Carla Gonzalez Miroslav Vranes Jörg Kämper Kyungyong Seong Ksenia Krasileva Regine Kahmann |
| author_facet | Mariana Schuster Gabriel Schweizer Stefanie Reißmann Petra Happel Daniela Aßmann Nicole Rössel Ulrich Güldener Gertrud Mannhaupt Nicole Ludwig Sarah Winterberg Clément Pellegrin Shigeyuki Tanaka Volker Vincon Libera Lo Presti Lei Wang Lena Bender Carla Gonzalez Miroslav Vranes Jörg Kämper Kyungyong Seong Ksenia Krasileva Regine Kahmann |
| author_sort | Mariana Schuster |
| collection | DOAJ |
| description | Fungal pathogens deploy a set of molecules (proteins, specialized metabolites, and sRNAs), so-called effectors, to aid the infection process. In comparison to other plant pathogens, smut fungi have small genomes and secretomes of 20 Mb and around 500 proteins, respectively. Previous comparative genomic studies have shown that many secreted effector proteins without known domains, i.e., novel, are conserved only in the Ustilaginaceae family. By analyzing the secretomes of 11 species within Ustilaginaceae, we identified 53 core homologous groups commonly present in this lineage. By collecting existing mutants and generating additional ones, we gathered 44 Ustilago maydis strains lacking single core effectors as well as 9 strains containing multiple deletions of core effector gene families. Pathogenicity assays revealed that 20 of these 53 mutant strains were affected in virulence. Among the 33 mutants that had no obvious phenotypic changes, 13 carried additional, sequence-divergent, structurally similar paralogs. We report a virulence contribution of seven previously uncharacterized single core effectors and of one effector family. Our results help to prioritize effectors for understanding U. maydis virulence and provide genetic resources for further characterization. [Graphic: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-04-24T13:18:16Z |
| format | Article |
| id | doaj.art-8387eeea8d864e2c90a2d31e6729d1cc |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-04-24T13:18:16Z |
| publishDate | 2024-03-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-8387eeea8d864e2c90a2d31e6729d1cc2024-04-04T17:01:39ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062024-03-0137325026310.1094/MPMI-09-23-0139-FINovel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydisMariana Schuster0Gabriel Schweizer1Stefanie Reißmann2Petra Happel3Daniela Aßmann4Nicole Rössel5Ulrich Güldener6Gertrud Mannhaupt7Nicole Ludwig8Sarah Winterberg9Clément Pellegrin10Shigeyuki Tanaka11Volker Vincon12Libera Lo Presti13Lei Wang14Lena Bender15Carla Gonzalez16Miroslav Vranes17Jörg Kämper18Kyungyong Seong19Ksenia Krasileva20Regine Kahmann21Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyDeutsches Herzzentrum München, Technische Universität München, 80636 München, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyMax Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyKarlsruhe Institute of Technology, Institute for Applied Biosciences, Department of Genetics, 76131 Karlsruhe, GermanyKarlsruhe Institute of Technology, Institute for Applied Biosciences, Department of Genetics, 76131 Karlsruhe, GermanyDepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720, U.S.A.Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, U.S.A.Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, GermanyFungal pathogens deploy a set of molecules (proteins, specialized metabolites, and sRNAs), so-called effectors, to aid the infection process. In comparison to other plant pathogens, smut fungi have small genomes and secretomes of 20 Mb and around 500 proteins, respectively. Previous comparative genomic studies have shown that many secreted effector proteins without known domains, i.e., novel, are conserved only in the Ustilaginaceae family. By analyzing the secretomes of 11 species within Ustilaginaceae, we identified 53 core homologous groups commonly present in this lineage. By collecting existing mutants and generating additional ones, we gathered 44 Ustilago maydis strains lacking single core effectors as well as 9 strains containing multiple deletions of core effector gene families. Pathogenicity assays revealed that 20 of these 53 mutant strains were affected in virulence. Among the 33 mutants that had no obvious phenotypic changes, 13 carried additional, sequence-divergent, structurally similar paralogs. We report a virulence contribution of seven previously uncharacterized single core effectors and of one effector family. Our results help to prioritize effectors for understanding U. maydis virulence and provide genetic resources for further characterization. [Graphic: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0139-FIbiotrophycomparative genomicsCRISPR-Cas9novel core effectorssmut fungiUstilago maydis |
| spellingShingle | Mariana Schuster Gabriel Schweizer Stefanie Reißmann Petra Happel Daniela Aßmann Nicole Rössel Ulrich Güldener Gertrud Mannhaupt Nicole Ludwig Sarah Winterberg Clément Pellegrin Shigeyuki Tanaka Volker Vincon Libera Lo Presti Lei Wang Lena Bender Carla Gonzalez Miroslav Vranes Jörg Kämper Kyungyong Seong Ksenia Krasileva Regine Kahmann Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis Molecular Plant-Microbe Interactions biotrophy comparative genomics CRISPR-Cas9 novel core effectors smut fungi Ustilago maydis |
| title | Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis |
| title_full | Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis |
| title_fullStr | Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis |
| title_full_unstemmed | Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis |
| title_short | Novel Secreted Effectors Conserved Among Smut Fungi Contribute to the Virulence of Ustilago maydis |
| title_sort | novel secreted effectors conserved among smut fungi contribute to the virulence of ustilago maydis |
| topic | biotrophy comparative genomics CRISPR-Cas9 novel core effectors smut fungi Ustilago maydis |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0139-FI |
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