Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic
Lotus japonicus is a well-studied nodulating legume and a model organism for the investigation of plant-microbe interactions. The majority of legume transcriptome studies have focused on interactions with compatible symbionts, whereas responses to non-adapted rhizobia and pathogenic bacteria have no...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2018-08-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2018.01218/full |
| _version_ | 1818321900416270336 |
|---|---|
| author | Simon Kelly Terry Mun Jens Stougaard Cécile Ben Stig U. Andersen |
| author_facet | Simon Kelly Terry Mun Jens Stougaard Cécile Ben Stig U. Andersen |
| author_sort | Simon Kelly |
| collection | DOAJ |
| description | Lotus japonicus is a well-studied nodulating legume and a model organism for the investigation of plant-microbe interactions. The majority of legume transcriptome studies have focused on interactions with compatible symbionts, whereas responses to non-adapted rhizobia and pathogenic bacteria have not been well-characterized. In this study, we first characterized the transcriptomic response of L. japonicus to its compatible symbiont, Mesorhizobium loti R7A, through RNA-seq analysis of various plant tissues. Early symbiotic signaling was largely Nod factor-dependent and enhanced within root hairs, and we observed large-scale transcriptional reprogramming in nodule primordia and mature nitrogen-fixing nodules. We then characterized root transcriptional responses to a spectrum of L. japonicus interacting bacteria ranging from semi-compatible symbionts to pathogens. M. loti R7A and the semi-compatible strain Sinorhizobium fredii HH103 showed remarkably similar responses, allowing us to identify a small number of genes potentially involved in differentiating between fully and semi-compatible symbionts. The incompatible symbiont Bradyrhizobium elkanii USDA61 induced a more attenuated response, but the weakest response was observed for the foliar pathogen Pseudomonas syringae pv. tomato DC3000, where the affected genes also responded to other tested bacteria, pointing to a small set of common bacterial response genes. In contrast, the root pathogen Ralstonia solanacearum JS763 induced a pronounced and distinct transcriptomic pathogen response, which we compared to the results of the other treatments. This comparative analysis did not support the concept that an early defense-like response is generally evoked by compatible rhizobia during establishment of symbiosis. |
| first_indexed | 2024-12-13T10:48:15Z |
| format | Article |
| id | doaj.art-f8c8a3e9bb7f4a07a6ccabc8a6236f7e |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-13T10:48:15Z |
| publishDate | 2018-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-f8c8a3e9bb7f4a07a6ccabc8a6236f7e2022-12-21T23:50:01ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-08-01910.3389/fpls.2018.01218377230Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to PathogenicSimon Kelly0Terry Mun1Jens Stougaard2Cécile Ben3Stig U. Andersen4Department of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkDepartment of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkDepartment of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkECOLAB, Université de Toulouse, CNRS, INP, UPS, Toulouse, FranceDepartment of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkLotus japonicus is a well-studied nodulating legume and a model organism for the investigation of plant-microbe interactions. The majority of legume transcriptome studies have focused on interactions with compatible symbionts, whereas responses to non-adapted rhizobia and pathogenic bacteria have not been well-characterized. In this study, we first characterized the transcriptomic response of L. japonicus to its compatible symbiont, Mesorhizobium loti R7A, through RNA-seq analysis of various plant tissues. Early symbiotic signaling was largely Nod factor-dependent and enhanced within root hairs, and we observed large-scale transcriptional reprogramming in nodule primordia and mature nitrogen-fixing nodules. We then characterized root transcriptional responses to a spectrum of L. japonicus interacting bacteria ranging from semi-compatible symbionts to pathogens. M. loti R7A and the semi-compatible strain Sinorhizobium fredii HH103 showed remarkably similar responses, allowing us to identify a small number of genes potentially involved in differentiating between fully and semi-compatible symbionts. The incompatible symbiont Bradyrhizobium elkanii USDA61 induced a more attenuated response, but the weakest response was observed for the foliar pathogen Pseudomonas syringae pv. tomato DC3000, where the affected genes also responded to other tested bacteria, pointing to a small set of common bacterial response genes. In contrast, the root pathogen Ralstonia solanacearum JS763 induced a pronounced and distinct transcriptomic pathogen response, which we compared to the results of the other treatments. This comparative analysis did not support the concept that an early defense-like response is generally evoked by compatible rhizobia during establishment of symbiosis.https://www.frontiersin.org/article/10.3389/fpls.2018.01218/fullsymbiosisnodulationRNA-seqpathogenlegumenitrogen fixation |
| spellingShingle | Simon Kelly Terry Mun Jens Stougaard Cécile Ben Stig U. Andersen Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic Frontiers in Plant Science symbiosis nodulation RNA-seq pathogen legume nitrogen fixation |
| title | Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic |
| title_full | Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic |
| title_fullStr | Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic |
| title_full_unstemmed | Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic |
| title_short | Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic |
| title_sort | distinct lotus japonicus transcriptomic responses to a spectrum of bacteria ranging from symbiotic to pathogenic |
| topic | symbiosis nodulation RNA-seq pathogen legume nitrogen fixation |
| url | https://www.frontiersin.org/article/10.3389/fpls.2018.01218/full |
| work_keys_str_mv | AT simonkelly distinctlotusjaponicustranscriptomicresponsestoaspectrumofbacteriarangingfromsymbiotictopathogenic AT terrymun distinctlotusjaponicustranscriptomicresponsestoaspectrumofbacteriarangingfromsymbiotictopathogenic AT jensstougaard distinctlotusjaponicustranscriptomicresponsestoaspectrumofbacteriarangingfromsymbiotictopathogenic AT cecileben distinctlotusjaponicustranscriptomicresponsestoaspectrumofbacteriarangingfromsymbiotictopathogenic AT stiguandersen distinctlotusjaponicustranscriptomicresponsestoaspectrumofbacteriarangingfromsymbiotictopathogenic |