Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency (original) (raw)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Institut des Sciences du Végétal, CNRS, 91198 Gif-sur-Yvette, France (V.L., M.S.R., F.L., H.B.-B., S.T.); Service de Bioénergétique Biologie Structurale et Mécanismes, Institut de Biologie et Technologies de Saclay, Commissariat à l'Energie Atomique Saclay, 91191 Gif-sur-Yvette, France (A.K.-L.); and University of Heidelberg, BIOQUANT 23, D–69120 Heidelberg, Germany (U.K.)

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Received:

13 November 2009

Accepted:

20 February 2010

Published:

24 February 2010

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Viviane Lanquar, Magali Schnell Ramos, Françoise Lelièvre, Hélène Barbier-Brygoo, Anja Krieger-Liszkay, Ute Krämer, Sébastien Thomine, Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency, Plant Physiology, Volume 152, Issue 4, April 2010, Pages 1986–1999, https://doi.org/10.1104/pp.109.150946
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Abstract

Manganese (Mn) is an essential element, acting as cofactor in numerous enzymes. In particular, a Mn cluster is indispensable for the function of the oxygen-evolving complex of photosystem II. Metal transporters of the Natural Resistance-Associated Macrophage Protein (NRAMP) family have the ability to transport both iron and Mn. AtNRAMP3 and AtNRAMP4 are required for iron mobilization in germinating seeds. The results reported here show that, in adult Arabidopsis (Arabidopsis thaliana) plants, AtNRAMP3 and AtNRAMP4 have an important role in Mn homeostasis. Vacuolar Mn accumulation in mesophyll cells of rosette leaves of adult nramp3nramp4 double mutant plants was dramatically increased when compared with the wild type. This suggests that a considerable proportion of the cellular Mn pool passes through the vacuole and is retrieved in an AtNRAMP3/AtNRAMP4-dependent manner. The impaired Mn release from mesophyll vacuoles of nramp3nramp4 double mutant plants is associated with reduced growth under Mn deficiency. However, leaf AtNRAMP3 and AtNRAMP4 protein levels are unaffected by Mn supply. Under Mn deficiency, nramp3nramp4 plants contain less functional photosystem II than the wild type. These data are consistent with a shortage of Mn to produce functional photosystem II, whereas mitochondrial Mn-dependent superoxide dismutase activity is maintained under Mn deficiency in both genotypes. The results presented here suggest an important role for AtNRAMP3/AtNRAMP4-dependent Mn transit through the vacuole prior to the import into chloroplasts of mesophyll cells.

© 2010 American Society of Plant Biologists

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