A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation
The response of Alnus glutinosa to Frankia alni ACN14a is driven by several sequential physiological events from calcium spiking and root-hair deformation to the development of the nodule. Early stages of actinorhizal symbiosis were monitored at the transcriptional level to observe plant host respon...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2022-12-01
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| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-06-22-0131-R |
| _version_ | 1811197770410754048 |
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| author | Mélanie Gasser Nicole Alloisio Pascale Fournier Severine Balmand Ons Kharrat Joris Tulumello Lorena Carro Abdelaziz Heddi Pedro Da Silva Philippe Normand Petar Pujic Hasna Boubakri |
| author_facet | Mélanie Gasser Nicole Alloisio Pascale Fournier Severine Balmand Ons Kharrat Joris Tulumello Lorena Carro Abdelaziz Heddi Pedro Da Silva Philippe Normand Petar Pujic Hasna Boubakri |
| author_sort | Mélanie Gasser |
| collection | DOAJ |
| description | The response of Alnus glutinosa to Frankia alni ACN14a is driven by several sequential physiological events from calcium spiking and root-hair deformation to the development of the nodule. Early stages of actinorhizal symbiosis were monitored at the transcriptional level to observe plant host responses to Frankia alni. Forty-two genes were significantly upregulated in inoculated compared with noninoculated roots. Most of these genes encode proteins involved in biological processes induced during microbial infection, such as oxidative stress or response to stimuli, but a large number of them are not differentially modulated or downregulated later in the process of nodulation. In contrast, several of them remained upregulated in mature nodules, and this included the gene most upregulated, which encodes a nonspecific lipid transfer protein (nsLTP). Classified as an antimicrobial peptide, this nsLTP was immunolocalized on the deformed root-hair surfaces that are points of contact for Frankia spp. during infection. Later in nodules, it binds to the surface of F. alni ACN14a vesicles, which are the specialized cells for nitrogen fixation. This nsLTP, named AgLTP24, was biologically produced in a heterologous host and purified for assay on F. alni ACN14a to identify physiological effects. Thus, the activation of the plant immunity response occurs upon first contact, while the recognition of F. alni ACN14a genes switches off part of the defense system during nodulation. AgLTP24 constitutes a part of the defense system that is maintained all along the symbiosis, with potential functions such as the formation of infection threads or nodule primordia to the control of F. alni proliferation. [Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-04-12T01:19:47Z |
| format | Article |
| id | doaj.art-7b7c42d593524ecca81e563c86f4cb1e |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-04-12T01:19:47Z |
| publishDate | 2022-12-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-7b7c42d593524ecca81e563c86f4cb1e2022-12-22T03:53:50ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062022-12-0135121096110810.1094/MPMI-06-22-0131-RA Nonspecific Lipid Transfer Protein with Potential Functions in Infection and NodulationMélanie Gasser0Nicole Alloisio1Pascale Fournier2Severine Balmand3Ons Kharrat4Joris Tulumello5Lorena Carro6Abdelaziz Heddi7Pedro Da Silva8Philippe Normand9Petar Pujic10Hasna Boubakri11Université de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceINSA-Lyon, INRAE, UMR203 BF2i, Biologie Fonctionnelle Insectes et Interactions, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceINSA-Lyon, INRAE, UMR203 BF2i, Biologie Fonctionnelle Insectes et Interactions, Villeurbanne, FranceINSA-Lyon, INRAE, UMR203 BF2i, Biologie Fonctionnelle Insectes et Interactions, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceUniversité de Lyon, F-69361, Lyon, France; Université Claude Bernard Lyon 1, CNRS, UMR 5557, INRAE UMR1418, Ecologie Microbienne, F-69622, Villeurbanne, FranceThe response of Alnus glutinosa to Frankia alni ACN14a is driven by several sequential physiological events from calcium spiking and root-hair deformation to the development of the nodule. Early stages of actinorhizal symbiosis were monitored at the transcriptional level to observe plant host responses to Frankia alni. Forty-two genes were significantly upregulated in inoculated compared with noninoculated roots. Most of these genes encode proteins involved in biological processes induced during microbial infection, such as oxidative stress or response to stimuli, but a large number of them are not differentially modulated or downregulated later in the process of nodulation. In contrast, several of them remained upregulated in mature nodules, and this included the gene most upregulated, which encodes a nonspecific lipid transfer protein (nsLTP). Classified as an antimicrobial peptide, this nsLTP was immunolocalized on the deformed root-hair surfaces that are points of contact for Frankia spp. during infection. Later in nodules, it binds to the surface of F. alni ACN14a vesicles, which are the specialized cells for nitrogen fixation. This nsLTP, named AgLTP24, was biologically produced in a heterologous host and purified for assay on F. alni ACN14a to identify physiological effects. Thus, the activation of the plant immunity response occurs upon first contact, while the recognition of F. alni ACN14a genes switches off part of the defense system during nodulation. AgLTP24 constitutes a part of the defense system that is maintained all along the symbiosis, with potential functions such as the formation of infection threads or nodule primordia to the control of F. alni proliferation. [Graphic: see text] Copyright © 2022 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-06-22-0131-RAlnus glutinosaantimicrobial peptideFrankiaimmunityinfection threadsnitrogen fixation |
| spellingShingle | Mélanie Gasser Nicole Alloisio Pascale Fournier Severine Balmand Ons Kharrat Joris Tulumello Lorena Carro Abdelaziz Heddi Pedro Da Silva Philippe Normand Petar Pujic Hasna Boubakri A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation Molecular Plant-Microbe Interactions Alnus glutinosa antimicrobial peptide Frankia immunity infection threads nitrogen fixation |
| title | A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation |
| title_full | A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation |
| title_fullStr | A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation |
| title_full_unstemmed | A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation |
| title_short | A Nonspecific Lipid Transfer Protein with Potential Functions in Infection and Nodulation |
| title_sort | nonspecific lipid transfer protein with potential functions in infection and nodulation |
| topic | Alnus glutinosa antimicrobial peptide Frankia immunity infection threads nitrogen fixation |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-06-22-0131-R |
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