Duplication of NRAMP3 gene in poplars generated two homologous transporters with distinct functions.

Arabidopsis Populus Salix Trans Golgi Network apoplasmic transport evolution manganese metal micronutrient nutrition recycling selective pressure symplasmic transport vacuole

Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
14 Jun 2022
Historique:
received: 15 12 2021
revised: 28 05 2022
accepted: 02 06 2022
entrez: 14 6 2022
pubmed: 15 6 2022
medline: 15 6 2022
Statut: aheadofprint

Résumé

Transition metals are essential for a wealth of metabolic reactions, but their concentrations need to be tightly controlled across cells and cell compartments, as metal excess or imbalance has deleterious effects. Metal homeostasis is achieved by a combination of metal transport across membranes and metal binding to a variety of molecules. Gene duplication is a key process in evolution, as emergence of advantageous mutations on one of the copies can confer a new function. Here, we report that the poplar genome contains two paralogues encoding NRAMP3 metal transporters localized in tandem. All Populus species analyzed had two copies of NRAMP3, whereas only one could be identified in Salix species indicating that duplication occurred when the two genera separated. Both copies are under purifying selection and encode functional transporters, as shown by expression in the yeast heterologous expression system. However, genetic complementation revealed that only one of the paralogues has retained the original function in release of metals stored in the vacuole previously characterized in A. thaliana. Confocal imaging showed that the other copy has acquired a distinct localization to the Trans Golgi Network (TGN). Expression in poplar suggested that the copy of NRAMP3 localized on the TGN has a novel function in the control of cell-to-cell transport of manganese. This work provides a clear case of neo-functionalization through change in the subcellular localization of a metal transporter as well as evidence for the involvement of the secretory pathway in cell-to-cell transport of manganese.

Identifiants

pubmed: 35700212
pii: 6608349
doi: 10.1093/molbev/msac129
pmc: PMC9234761
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

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Auteurs

Mathieu Pottier (M)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.
Current affiliation: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany.

Van Anh Le Thi (VA)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.
Current affiliation: Graduate University of Science and Technology (GUST), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet, Cau Giay, Hanoi 10000, Vietnam.

Catherine Primard-Brisset (C)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.

Jessica Marion (J)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.

Michele Bianchi (M)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.

Cindy Victor (C)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.

Annabelle Déjardin (A)

INRAE, ONF, BioForA, Orléans, France.

Gilles Pilate (G)

INRAE, ONF, BioForA, Orléans, France.

Sébastien Thomine (S)

Institut de Biologie Intégrative de la Cellule, CNRS, Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.

Classifications MeSH