Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction

Nitrogen (N) as well as Phosphorus (P) are key nutrients determining crop productivity. Legumes have developed strategies to overcome nutrient limitation by, for example, forming a symbiotic relationship with N-fixing rhizobia and the release of P-mobilizing exudates and are thus able to grow withou...

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Main Authors: Wanda Biała-Leonhard, Laura Zanin, Stefano Gottardi, Rita de Brito Francisco, Silvia Venuti, Fabio Valentinuzzi, Tanja Mimmo, Stefano Cesco, Barbara Bassin, Enrico Martinoia, Roberto Pinton, Michał Jasiński, Nicola Tomasi
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.758213/full
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author Wanda Biała-Leonhard
Laura Zanin
Stefano Gottardi
Rita de Brito Francisco
Silvia Venuti
Fabio Valentinuzzi
Fabio Valentinuzzi
Tanja Mimmo
Stefano Cesco
Barbara Bassin
Enrico Martinoia
Enrico Martinoia
Roberto Pinton
Michał Jasiński
Michał Jasiński
Nicola Tomasi
author_facet Wanda Biała-Leonhard
Laura Zanin
Stefano Gottardi
Rita de Brito Francisco
Silvia Venuti
Fabio Valentinuzzi
Fabio Valentinuzzi
Tanja Mimmo
Stefano Cesco
Barbara Bassin
Enrico Martinoia
Enrico Martinoia
Roberto Pinton
Michał Jasiński
Michał Jasiński
Nicola Tomasi
author_sort Wanda Biała-Leonhard
collection DOAJ
description Nitrogen (N) as well as Phosphorus (P) are key nutrients determining crop productivity. Legumes have developed strategies to overcome nutrient limitation by, for example, forming a symbiotic relationship with N-fixing rhizobia and the release of P-mobilizing exudates and are thus able to grow without supply of N or P fertilizers. The legume-rhizobial symbiosis starts with root release of isoflavonoids that act as signaling molecules perceived by compatible bacteria. Subsequently, bacteria release nod factors, which induce signaling cascades allowing the formation of functional N-fixing nodules. We report here the identification and functional characterization of a plasma membrane-localized MATE-type transporter (LaMATE2) involved in the release of genistein from white lupin roots. The LaMATE2 expression in the root is upregulated under N deficiency as well as low phosphate availability, two nutritional deficiencies that induce the release of this isoflavonoid. LaMATE2 silencing reduced genistein efflux and even more the formation of symbiotic nodules, supporting the crucial role of LaMATE2 in isoflavonoid release and nodulation. Furthermore, silencing of LaMATE2 limited the P-solubilization activity of lupin root exudates. Transport assays in yeast vesicles demonstrated that LaMATE2 acts as a proton-driven isoflavonoid transporter.
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spelling doaj.art-5527de94f54c44cc9c2ca5b9bd8bc5b22022-12-21T20:36:01ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-10-011210.3389/fpls.2021.758213758213Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic InteractionWanda Biała-Leonhard0Laura Zanin1Stefano Gottardi2Rita de Brito Francisco3Silvia Venuti4Fabio Valentinuzzi5Fabio Valentinuzzi6Tanja Mimmo7Stefano Cesco8Barbara Bassin9Enrico Martinoia10Enrico Martinoia11Roberto Pinton12Michał Jasiński13Michał Jasiński14Nicola Tomasi15Department of Plant Molecular Physiology, Polish Academy of Sciences, Institute of Bioorganic Chemistry, Poznań, PolandDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyInstitute of Plant and Microbial Biology, University of Zurich, Zurich, SwitzerlandDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyFaculty of Science and Technology, Free University of Bozen Bolzano, Bolzano, ItalyFaculty of Science and Technology, Free University of Bozen Bolzano, Bolzano, ItalyFaculty of Science and Technology, Free University of Bozen Bolzano, Bolzano, ItalyInstitute of Plant and Microbial Biology, University of Zurich, Zurich, SwitzerlandInstitute of Plant and Microbial Biology, University of Zurich, Zurich, SwitzerlandInternational Research Center for Environmental Membrane Biology, Foshan University, Foshan, ChinaDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyDepartment of Plant Molecular Physiology, Polish Academy of Sciences, Institute of Bioorganic Chemistry, Poznań, PolandDepartment of Biochemistry and Biotechnology, Poznań University of Life Sciences, Poznań, PolandDipartimento di Scienze Agro-Alimentari, Ambientali e Animali, University of Udine, Udine, ItalyNitrogen (N) as well as Phosphorus (P) are key nutrients determining crop productivity. Legumes have developed strategies to overcome nutrient limitation by, for example, forming a symbiotic relationship with N-fixing rhizobia and the release of P-mobilizing exudates and are thus able to grow without supply of N or P fertilizers. The legume-rhizobial symbiosis starts with root release of isoflavonoids that act as signaling molecules perceived by compatible bacteria. Subsequently, bacteria release nod factors, which induce signaling cascades allowing the formation of functional N-fixing nodules. We report here the identification and functional characterization of a plasma membrane-localized MATE-type transporter (LaMATE2) involved in the release of genistein from white lupin roots. The LaMATE2 expression in the root is upregulated under N deficiency as well as low phosphate availability, two nutritional deficiencies that induce the release of this isoflavonoid. LaMATE2 silencing reduced genistein efflux and even more the formation of symbiotic nodules, supporting the crucial role of LaMATE2 in isoflavonoid release and nodulation. Furthermore, silencing of LaMATE2 limited the P-solubilization activity of lupin root exudates. Transport assays in yeast vesicles demonstrated that LaMATE2 acts as a proton-driven isoflavonoid transporter.https://www.frontiersin.org/articles/10.3389/fpls.2021.758213/fullBradyrhizobiumgenisteinLupinus albusMATE transporternitrogenphosphorus
spellingShingle Wanda Biała-Leonhard
Laura Zanin
Stefano Gottardi
Rita de Brito Francisco
Silvia Venuti
Fabio Valentinuzzi
Fabio Valentinuzzi
Tanja Mimmo
Stefano Cesco
Barbara Bassin
Enrico Martinoia
Enrico Martinoia
Roberto Pinton
Michał Jasiński
Michał Jasiński
Nicola Tomasi
Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
Frontiers in Plant Science
Bradyrhizobium
genistein
Lupinus albus
MATE transporter
nitrogen
phosphorus
title Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
title_full Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
title_fullStr Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
title_full_unstemmed Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
title_short Identification of an Isoflavonoid Transporter Required for the Nodule Establishment of the Rhizobium-Fabaceae Symbiotic Interaction
title_sort identification of an isoflavonoid transporter required for the nodule establishment of the rhizobium fabaceae symbiotic interaction
topic Bradyrhizobium
genistein
Lupinus albus
MATE transporter
nitrogen
phosphorus
url https://www.frontiersin.org/articles/10.3389/fpls.2021.758213/full
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