Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i>
The transmission of seed-borne pathogens by the germinating seed is responsible for major crop diseases. The immune responses of the seed facing biotic invaders are poorly documented so far. The <i>Arabidopsis thaliana</i>/<i>Alternaria brassicicola</i> patho-system was used...
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MDPI AG
2022-06-01
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| Series: | Plants |
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| Online Access: | https://www.mdpi.com/2223-7747/11/13/1708 |
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| author | Mailen Ortega-Cuadros Tiago Lodi De Souza Romain Berruyer Sophie Aligon Sandra Pelletier Jean-Pierre Renou Tatiana Arias Claire Campion Thomas Guillemette Jérome Verdier Philippe Grappin |
| author_facet | Mailen Ortega-Cuadros Tiago Lodi De Souza Romain Berruyer Sophie Aligon Sandra Pelletier Jean-Pierre Renou Tatiana Arias Claire Campion Thomas Guillemette Jérome Verdier Philippe Grappin |
| author_sort | Mailen Ortega-Cuadros |
| collection | DOAJ |
| description | The transmission of seed-borne pathogens by the germinating seed is responsible for major crop diseases. The immune responses of the seed facing biotic invaders are poorly documented so far. The <i>Arabidopsis thaliana</i>/<i>Alternaria brassicicola</i> patho-system was used to describe at the transcription level the responses of germinating seeds and young seedling stages to infection by the necrotrophic fungus. RNA-seq analyses of healthy versus inoculated seeds at 3 days after sowing (DAS), stage of radicle emergence, and at 6 and 10 DAS, two stages of seedling establishment, identified thousands of differentially expressed genes by <i>Alternaria</i> infection. Response to hypoxia, ethylene and indole pathways were found to be induced by <i>Alternaria</i> in the germinating seeds. However, surprisingly, the defense responses, namely the salicylic acid (SA) pathway, the response to reactive oxygen species (ROS), the endoplasmic reticulum-associated protein degradation (ERAD) and programmed cell death, were found to be strongly induced only during the latter post-germination stages. We propose that this non-canonical immune response in early germinating seeds compared to early seedling establishment was potentially due to the seed-to-seedling transition phase. Phenotypic analyses of about 14 mutants altered in the main defense pathways illustrated these specific defense responses. The unexpected germination deficiency and insensitivity to <i>Alternaria</i> in the glucosinolate deficient mutants allow hypothesis of a trade-off between seed germination, necrosis induction and <i>Alternaria</i> transmission to the seedling. The imbalance of the SA and jasmonic acid (JA) pathways to the detriment of the JA also illustrated a non-canonical immune response at the first stages of the seedling. |
| first_indexed | 2024-03-09T03:57:33Z |
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| id | doaj.art-75e6b1f7ebb44493b97da4f11b776ec1 |
| institution | Directory Open Access Journal |
| issn | 2223-7747 |
| language | English |
| last_indexed | 2024-03-09T03:57:33Z |
| publishDate | 2022-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Plants |
| spelling | doaj.art-75e6b1f7ebb44493b97da4f11b776ec12023-12-03T14:17:48ZengMDPI AGPlants2223-77472022-06-011113170810.3390/plants11131708Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i>Mailen Ortega-Cuadros0Tiago Lodi De Souza1Romain Berruyer2Sophie Aligon3Sandra Pelletier4Jean-Pierre Renou5Tatiana Arias6Claire Campion7Thomas Guillemette8Jérome Verdier9Philippe Grappin10Faculty of Exact and Natural Sciences, Institute of Biology, University City Campus, University of Antioquia, Calle 67 N°53-108, Medellín 050010, ColombiaInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceMarie Selby Botanical Gardens, Downtown Sarasota Campus, 1534 Mound Street, Sarasota, FL 34236, USAInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceInstitut Agro, University Angers, INRAE, IRHS, SFR 4207 QuaSaV, F-49000 Angers, FranceThe transmission of seed-borne pathogens by the germinating seed is responsible for major crop diseases. The immune responses of the seed facing biotic invaders are poorly documented so far. The <i>Arabidopsis thaliana</i>/<i>Alternaria brassicicola</i> patho-system was used to describe at the transcription level the responses of germinating seeds and young seedling stages to infection by the necrotrophic fungus. RNA-seq analyses of healthy versus inoculated seeds at 3 days after sowing (DAS), stage of radicle emergence, and at 6 and 10 DAS, two stages of seedling establishment, identified thousands of differentially expressed genes by <i>Alternaria</i> infection. Response to hypoxia, ethylene and indole pathways were found to be induced by <i>Alternaria</i> in the germinating seeds. However, surprisingly, the defense responses, namely the salicylic acid (SA) pathway, the response to reactive oxygen species (ROS), the endoplasmic reticulum-associated protein degradation (ERAD) and programmed cell death, were found to be strongly induced only during the latter post-germination stages. We propose that this non-canonical immune response in early germinating seeds compared to early seedling establishment was potentially due to the seed-to-seedling transition phase. Phenotypic analyses of about 14 mutants altered in the main defense pathways illustrated these specific defense responses. The unexpected germination deficiency and insensitivity to <i>Alternaria</i> in the glucosinolate deficient mutants allow hypothesis of a trade-off between seed germination, necrosis induction and <i>Alternaria</i> transmission to the seedling. The imbalance of the SA and jasmonic acid (JA) pathways to the detriment of the JA also illustrated a non-canonical immune response at the first stages of the seedling.https://www.mdpi.com/2223-7747/11/13/1708<i>Arabidopsis</i><i>Alternaria brassicicola</i>seed-borne pathogen transmissionsusceptible response |
| spellingShingle | Mailen Ortega-Cuadros Tiago Lodi De Souza Romain Berruyer Sophie Aligon Sandra Pelletier Jean-Pierre Renou Tatiana Arias Claire Campion Thomas Guillemette Jérome Verdier Philippe Grappin Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> Plants <i>Arabidopsis</i> <i>Alternaria brassicicola</i> seed-borne pathogen transmission susceptible response |
| title | Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> |
| title_full | Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> |
| title_fullStr | Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> |
| title_full_unstemmed | Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> |
| title_short | Seed Transmission of Pathogens: Non-Canonical Immune Response in <i>Arabidopsis</i> Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus <i>Alternaria brassicicola</i> |
| title_sort | seed transmission of pathogens non canonical immune response in i arabidopsis i germinating seeds compared to early seedlings against the necrotrophic fungus i alternaria brassicicola i |
| topic | <i>Arabidopsis</i> <i>Alternaria brassicicola</i> seed-borne pathogen transmission susceptible response |
| url | https://www.mdpi.com/2223-7747/11/13/1708 |
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