Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses
Rust fungi are devastating pathogens for several important crop plants. The biotrophic lifestyle of rust fungi requires that they influence their host plants to create a favorable environment for growth and reproduction. Rust fungi secrete a variety of effector proteins that manipulate host target p...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-10-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.01182/full |
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| author | Mingsheng Qi Yu Mei James P. Grayczyk Luana M. Darben Martin E. G. Rieker Janina M. Seitz Ralf T. Voegele Steven A. Whitham Tobias I. Link |
| author_facet | Mingsheng Qi Yu Mei James P. Grayczyk Luana M. Darben Martin E. G. Rieker Janina M. Seitz Ralf T. Voegele Steven A. Whitham Tobias I. Link |
| author_sort | Mingsheng Qi |
| collection | DOAJ |
| description | Rust fungi are devastating pathogens for several important crop plants. The biotrophic lifestyle of rust fungi requires that they influence their host plants to create a favorable environment for growth and reproduction. Rust fungi secrete a variety of effector proteins that manipulate host target proteins to alter plant metabolism and suppress defense responses. Because of the obligate biotrophic lifestyle of rust fungi, direct evidence for effector function is difficult to obtain, and so suites of experiments utilizing expression in heterologous systems are necessary. Here, we present results from a yeast cell death suppression assay and assays for suppression of PAMP-triggered immunity (PTI) and effector triggered immunity (ETI) based on delivery of effectors through the bacterial type III secretion system. In addition, subcellular localization was tested using transient expression of GFP fusion proteins in Nicotiana benthamiana through Agrobacterium infiltration. We tested 31 representative effector candidates from the devastating common bean rust pathogen Uromyces appendiculatus. These effector candidates were selected based on features of their gene families, most important lineage specificity. We show that several of our effector candidates suppress plant defense. Some of them also belong to families of effector candidates that are present in multiple rust species where their homologs probably also have effector functions. In our analysis of candidate effector mRNA expression, some of those effector candidates that gave positive results in the other assays were not up-regulated during plant infection, indicating that either these proteins have functions at multiple life stages or that strong up-regulation of RNA level in planta may not be as important a criterion for identifying effectors as previously thought. Overall, our pipeline for selecting effector candidates based on sequence features followed by screening assays using heterologous expression systems was successful in discriminating effector candidates. This work lays the foundation for functional characterization of U. appendiculatus effectors, the identification of effector targets, and identification of novel sources for resistance in common bean. |
| first_indexed | 2024-12-11T11:39:55Z |
| format | Article |
| id | doaj.art-45c2b3c4cceb4e83b179760ad5e0280e |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-11T11:39:55Z |
| publishDate | 2019-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-45c2b3c4cceb4e83b179760ad5e0280e2022-12-22T01:08:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-10-011010.3389/fpls.2019.01182474937Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune ResponsesMingsheng Qi0Yu Mei1James P. Grayczyk2Luana M. Darben3Martin E. G. Rieker4Janina M. Seitz5Ralf T. Voegele6Steven A. Whitham7Tobias I. Link8Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesDepartment of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesDepartment of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesPlant Biotechnology, Embrapa Soja, Londrina, BrazilInstitut für Phytomedizin, Universität Hohenheim, Stuttgart, GermanyInstitut für Phytomedizin, Universität Hohenheim, Stuttgart, GermanyInstitut für Phytomedizin, Universität Hohenheim, Stuttgart, GermanyDepartment of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesInstitut für Phytomedizin, Universität Hohenheim, Stuttgart, GermanyRust fungi are devastating pathogens for several important crop plants. The biotrophic lifestyle of rust fungi requires that they influence their host plants to create a favorable environment for growth and reproduction. Rust fungi secrete a variety of effector proteins that manipulate host target proteins to alter plant metabolism and suppress defense responses. Because of the obligate biotrophic lifestyle of rust fungi, direct evidence for effector function is difficult to obtain, and so suites of experiments utilizing expression in heterologous systems are necessary. Here, we present results from a yeast cell death suppression assay and assays for suppression of PAMP-triggered immunity (PTI) and effector triggered immunity (ETI) based on delivery of effectors through the bacterial type III secretion system. In addition, subcellular localization was tested using transient expression of GFP fusion proteins in Nicotiana benthamiana through Agrobacterium infiltration. We tested 31 representative effector candidates from the devastating common bean rust pathogen Uromyces appendiculatus. These effector candidates were selected based on features of their gene families, most important lineage specificity. We show that several of our effector candidates suppress plant defense. Some of them also belong to families of effector candidates that are present in multiple rust species where their homologs probably also have effector functions. In our analysis of candidate effector mRNA expression, some of those effector candidates that gave positive results in the other assays were not up-regulated during plant infection, indicating that either these proteins have functions at multiple life stages or that strong up-regulation of RNA level in planta may not be as important a criterion for identifying effectors as previously thought. Overall, our pipeline for selecting effector candidates based on sequence features followed by screening assays using heterologous expression systems was successful in discriminating effector candidates. This work lays the foundation for functional characterization of U. appendiculatus effectors, the identification of effector targets, and identification of novel sources for resistance in common bean.https://www.frontiersin.org/article/10.3389/fpls.2019.01182/fullUromyces appendiculatuseffectorsPTI suppressionETI suppressionbax cell death suppressionlocalization |
| spellingShingle | Mingsheng Qi Yu Mei James P. Grayczyk Luana M. Darben Martin E. G. Rieker Janina M. Seitz Ralf T. Voegele Steven A. Whitham Tobias I. Link Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses Frontiers in Plant Science Uromyces appendiculatus effectors PTI suppression ETI suppression bax cell death suppression localization |
| title | Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses |
| title_full | Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses |
| title_fullStr | Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses |
| title_full_unstemmed | Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses |
| title_short | Candidate Effectors From Uromyces appendiculatus, the Causal Agent of Rust on Common Bean, Can Be Discriminated Based on Suppression of Immune Responses |
| title_sort | candidate effectors from uromyces appendiculatus the causal agent of rust on common bean can be discriminated based on suppression of immune responses |
| topic | Uromyces appendiculatus effectors PTI suppression ETI suppression bax cell death suppression localization |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.01182/full |
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