The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance

Arbuscular mycorrhizal fungi increase fitness of their host plants under Cu deficient and toxic conditions. In this study, we have characterized two Cu transporters of the CTR family (RiCTR1 and RiCTR2) and a CTR-like protein (RiCTR3A) of Rhizophagus irregularis. Functional analyses in yeast reveale...

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Main Authors: Tamara Gómez-Gallego, Karim Benabdellah, Miguel A. Merlos, Ana M. Jiménez-Jiménez, Carine Alcon, Pierre Berthomieu, Nuria Ferrol
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00604/full
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author Tamara Gómez-Gallego
Karim Benabdellah
Miguel A. Merlos
Ana M. Jiménez-Jiménez
Carine Alcon
Pierre Berthomieu
Nuria Ferrol
author_facet Tamara Gómez-Gallego
Karim Benabdellah
Miguel A. Merlos
Ana M. Jiménez-Jiménez
Carine Alcon
Pierre Berthomieu
Nuria Ferrol
author_sort Tamara Gómez-Gallego
collection DOAJ
description Arbuscular mycorrhizal fungi increase fitness of their host plants under Cu deficient and toxic conditions. In this study, we have characterized two Cu transporters of the CTR family (RiCTR1 and RiCTR2) and a CTR-like protein (RiCTR3A) of Rhizophagus irregularis. Functional analyses in yeast revealed that RiCTR1 encodes a plasma membrane Cu transporter, RiCTR2 a vacuolar Cu transporter and RiCTR3A a plasma membrane protein involved in Cu tolerance. RiCTR1 was more highly expressed in the extraradical mycelia (ERM) and RiCTR2 in the intraradical mycelia (IRM). In the ERM, RiCTR1 expression was up-regulated by Cu deficiency and down-regulated by Cu toxicity. RiCTR2 expression increased only in the ERM grown under severe Cu-deficient conditions. These data suggest that RiCTR1 is involved in Cu uptake by the ERM and RiCTR2 in mobilization of vacuolar Cu stores. Cu deficiency decreased mycorrhizal colonization and arbuscule frequency, but increased RiCTR1 and RiCTR2 expression in the IRM, which suggest that the IRM has a high Cu demand. The two alternatively spliced products of RiCTR3, RiCTR3A and RiCTR3B, were more highly expressed in the ERM. Up-regulation of RiCTR3A by Cu toxicity and the yeast complementation assays suggest that RiCTR3A might function as a Cu receptor involved in Cu tolerance.
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spelling doaj.art-a5695e4a971e4b39ad3d04628907ef982022-12-22T03:00:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-05-011010.3389/fpls.2019.00604456471The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper ToleranceTamara Gómez-Gallego0Karim Benabdellah1Miguel A. Merlos2Ana M. Jiménez-Jiménez3Carine Alcon4Pierre Berthomieu5Nuria Ferrol6Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainGenomic Medicine Department, GENYO, Centre for Genomics and Oncological Research, Pfizer-University of Granada-Andalusian Regional Government, Granada, SpainDepartamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainBiochimie et Physiologie Moléculaire des Plantes, Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique, Université de Montpellier, Montpellier SupAgro, Montpellier, FranceBiochimie et Physiologie Moléculaire des Plantes, Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique, Université de Montpellier, Montpellier SupAgro, Montpellier, FranceDepartamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainArbuscular mycorrhizal fungi increase fitness of their host plants under Cu deficient and toxic conditions. In this study, we have characterized two Cu transporters of the CTR family (RiCTR1 and RiCTR2) and a CTR-like protein (RiCTR3A) of Rhizophagus irregularis. Functional analyses in yeast revealed that RiCTR1 encodes a plasma membrane Cu transporter, RiCTR2 a vacuolar Cu transporter and RiCTR3A a plasma membrane protein involved in Cu tolerance. RiCTR1 was more highly expressed in the extraradical mycelia (ERM) and RiCTR2 in the intraradical mycelia (IRM). In the ERM, RiCTR1 expression was up-regulated by Cu deficiency and down-regulated by Cu toxicity. RiCTR2 expression increased only in the ERM grown under severe Cu-deficient conditions. These data suggest that RiCTR1 is involved in Cu uptake by the ERM and RiCTR2 in mobilization of vacuolar Cu stores. Cu deficiency decreased mycorrhizal colonization and arbuscule frequency, but increased RiCTR1 and RiCTR2 expression in the IRM, which suggest that the IRM has a high Cu demand. The two alternatively spliced products of RiCTR3, RiCTR3A and RiCTR3B, were more highly expressed in the ERM. Up-regulation of RiCTR3A by Cu toxicity and the yeast complementation assays suggest that RiCTR3A might function as a Cu receptor involved in Cu tolerance.https://www.frontiersin.org/article/10.3389/fpls.2019.00604/fullarbuscular mycorrhizal fungicopper homeostasiscopper transportersCTR familyRhizophagus irregularissymbiosis
spellingShingle Tamara Gómez-Gallego
Karim Benabdellah
Miguel A. Merlos
Ana M. Jiménez-Jiménez
Carine Alcon
Pierre Berthomieu
Nuria Ferrol
The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
Frontiers in Plant Science
arbuscular mycorrhizal fungi
copper homeostasis
copper transporters
CTR family
Rhizophagus irregularis
symbiosis
title The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
title_full The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
title_fullStr The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
title_full_unstemmed The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
title_short The Rhizophagus irregularis Genome Encodes Two CTR Copper Transporters That Mediate Cu Import Into the Cytosol and a CTR-Like Protein Likely Involved in Copper Tolerance
title_sort rhizophagus irregularis genome encodes two ctr copper transporters that mediate cu import into the cytosol and a ctr like protein likely involved in copper tolerance
topic arbuscular mycorrhizal fungi
copper homeostasis
copper transporters
CTR family
Rhizophagus irregularis
symbiosis
url https://www.frontiersin.org/article/10.3389/fpls.2019.00604/full
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