Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function

Several aspects of the legume–rhizobia symbiosis are far from being completely understood, such as the transport of compounds through the symbiosome membrane and the molecular actors (receptors, transcription factors and hormones) involved in the systemic regulation of nodulation. In this work, the...

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Main Authors: Carmen M. Pérez-Delgado, Margarita García-Calderón, María Dolores Monje-Rueda, Antonio J. Márquez, Marco Betti
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Agronomy
Subjects:
Online Access:https://www.mdpi.com/2073-4395/10/6/819
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author Carmen M. Pérez-Delgado
Margarita García-Calderón
María Dolores Monje-Rueda
Antonio J. Márquez
Marco Betti
author_facet Carmen M. Pérez-Delgado
Margarita García-Calderón
María Dolores Monje-Rueda
Antonio J. Márquez
Marco Betti
author_sort Carmen M. Pérez-Delgado
collection DOAJ
description Several aspects of the legume–rhizobia symbiosis are far from being completely understood, such as the transport of compounds through the symbiosome membrane and the molecular actors (receptors, transcription factors and hormones) involved in the systemic regulation of nodulation. In this work, the transcriptomes of <i>L. japonicus</i> plants growing under symbiotic or non-symbiotic conditions were studied in roots and shoots, in order to look for new genes involved in nodule function and regulation both at the local and systemic levels. Several of the genes differentially expressed in roots were well-known nodulins; however, other genes with unknown function were also discovered that showed univocal nodule-specific expression profiles. Transporters of the Nitrate Transporter1/Peptide Transporter Family family, putative oligopeptide transporters, as well as other uncharacterized transporters were upregulated in nodulated roots. Five transcription factors, as well as receptors/kinases and an f-box domain containing protein, all of unknown function, were also more upregulated in nodulated roots. In the shoots of nodulated plants, genes involved in jasmonic acid and indole-3-acetic acid metabolism were differentially expressed. Moreover, three genes encoding for different glutaredoxins, proteins that were recently involved in the systemic signaling of the Arabidopsis nitrogen status, were highly downregulated in the leaves of nodulated plants. Protein–protein interaction network analysis identified nitrate reductase as a central hub in nitrogen metabolism, and a putative protein of the NADH-ubiquinone complex was highly connected to several SWEET transporters. Clustering analysis of the differentially expressed genes also suggested a possible role for a previously uncharacterized ethylene-responsive transcription factor and for LBD38 homologs in <i>L. japonicus</i> nodule function. The new genes identified in this study represent a promising target for the understating and manipulation of symbiotic nitrogen fixation, with the aim of improving crop legumes’ productivity.
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spelling doaj.art-f221123d0bd847e7b5653ce5f5caf7202023-11-20T03:19:58ZengMDPI AGAgronomy2073-43952020-06-0110681910.3390/agronomy10060819Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule FunctionCarmen M. Pérez-Delgado0Margarita García-Calderón1María Dolores Monje-Rueda2Antonio J. Márquez3Marco Betti4Departamento de Bioquímica Vegetal y Biología Molecular, Facultad de Química, Calle Prof. García González, 1, 41012 Sevilla, SpainDepartamento de Bioquímica Vegetal y Biología Molecular, Facultad de Química, Calle Prof. García González, 1, 41012 Sevilla, SpainDepartamento de Bioquímica Vegetal y Biología Molecular, Facultad de Química, Calle Prof. García González, 1, 41012 Sevilla, SpainDepartamento de Bioquímica Vegetal y Biología Molecular, Facultad de Química, Calle Prof. García González, 1, 41012 Sevilla, SpainDepartamento de Bioquímica Vegetal y Biología Molecular, Facultad de Química, Calle Prof. García González, 1, 41012 Sevilla, SpainSeveral aspects of the legume–rhizobia symbiosis are far from being completely understood, such as the transport of compounds through the symbiosome membrane and the molecular actors (receptors, transcription factors and hormones) involved in the systemic regulation of nodulation. In this work, the transcriptomes of <i>L. japonicus</i> plants growing under symbiotic or non-symbiotic conditions were studied in roots and shoots, in order to look for new genes involved in nodule function and regulation both at the local and systemic levels. Several of the genes differentially expressed in roots were well-known nodulins; however, other genes with unknown function were also discovered that showed univocal nodule-specific expression profiles. Transporters of the Nitrate Transporter1/Peptide Transporter Family family, putative oligopeptide transporters, as well as other uncharacterized transporters were upregulated in nodulated roots. Five transcription factors, as well as receptors/kinases and an f-box domain containing protein, all of unknown function, were also more upregulated in nodulated roots. In the shoots of nodulated plants, genes involved in jasmonic acid and indole-3-acetic acid metabolism were differentially expressed. Moreover, three genes encoding for different glutaredoxins, proteins that were recently involved in the systemic signaling of the Arabidopsis nitrogen status, were highly downregulated in the leaves of nodulated plants. Protein–protein interaction network analysis identified nitrate reductase as a central hub in nitrogen metabolism, and a putative protein of the NADH-ubiquinone complex was highly connected to several SWEET transporters. Clustering analysis of the differentially expressed genes also suggested a possible role for a previously uncharacterized ethylene-responsive transcription factor and for LBD38 homologs in <i>L. japonicus</i> nodule function. The new genes identified in this study represent a promising target for the understating and manipulation of symbiotic nitrogen fixation, with the aim of improving crop legumes’ productivity.https://www.mdpi.com/2073-4395/10/6/819transcriptomicsrhizobial symbiosissymbiotic nitrogen fixationlegume productivitysystemic signaling<i>Lotus japonicus</i>
spellingShingle Carmen M. Pérez-Delgado
Margarita García-Calderón
María Dolores Monje-Rueda
Antonio J. Márquez
Marco Betti
Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
Agronomy
transcriptomics
rhizobial symbiosis
symbiotic nitrogen fixation
legume productivity
systemic signaling
<i>Lotus japonicus</i>
title Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
title_full Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
title_fullStr Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
title_full_unstemmed Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
title_short Transcriptomic Analysis of <i>L. japonicus</i> Symbiosis Reveals New Candidate Genes for Local and Systemic Regulation of Nodule Function
title_sort transcriptomic analysis of i l japonicus i symbiosis reveals new candidate genes for local and systemic regulation of nodule function
topic transcriptomics
rhizobial symbiosis
symbiotic nitrogen fixation
legume productivity
systemic signaling
<i>Lotus japonicus</i>
url https://www.mdpi.com/2073-4395/10/6/819
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