AtDTX25, a member of the multidrug and toxic compound extrusion family, is a vacuolar ascorbate transporter that controls intracellular iron cycling in Arabidopsis

Summary Iron (Fe) is an essential element, its transport is regulated by the cell redox balance. In seeds, Fe enters the embryo as Fe2+ and is stored in vacuoles as Fe3+. Through its ferric reduction activity, ascorbate plays a major role in Fe redox state and therefore Fe transport within the seed....

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Veröffentlicht in:The New phytologist 2021-09, Vol.231 (5), p.1956-1967
Hauptverfasser: Hoang, Minh Thi Thanh, Almeida, Diego, Chay, Sandrine, Alcon, Carine, Corratge‐Faillie, Claire, Curie, Catherine, Mari, Stephane
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container_end_page 1967
container_issue 5
container_start_page 1956
container_title The New phytologist
container_volume 231
creator Hoang, Minh Thi Thanh
Almeida, Diego
Chay, Sandrine
Alcon, Carine
Corratge‐Faillie, Claire
Curie, Catherine
Mari, Stephane
description Summary Iron (Fe) is an essential element, its transport is regulated by the cell redox balance. In seeds, Fe enters the embryo as Fe2+ and is stored in vacuoles as Fe3+. Through its ferric reduction activity, ascorbate plays a major role in Fe redox state and therefore Fe transport within the seed. We searched for ascorbate membrane transporters responsible for controlling Fe reduction by screening the yeast ferric reductase‐deficient fre1 strain and isolated AtDTX25, a member of the Multidrug And Toxic compound Extrusion (MATE) family. AtDTX25 was shown to mediate ascorbate efflux when expressed in yeast and Xenopus oocytes, in a pH‐dependent manner. In planta, AtDTX25 is highly expressed during germination and encodes a vacuolar membrane protein. Isolated vacuoles from AtDTX25‐1 knockout mutant contained less ascorbate and more Fe than wild‐type (WT), and mutant seedlings were highly sensitive to Fe deficiency. Iron imaging further showed that the remobilisation of Fe from vacuoles was highly impaired in mutant seedlings. Taken together, our results established AtDTX25 as a vacuolar ascorbate transporter, required during germination to promote the reduction of the pool of stored Fe3+ and its remobilisation to feed the developing seedling.
doi_str_mv 10.1111/nph.17526
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In seeds, Fe enters the embryo as Fe2+ and is stored in vacuoles as Fe3+. Through its ferric reduction activity, ascorbate plays a major role in Fe redox state and therefore Fe transport within the seed. We searched for ascorbate membrane transporters responsible for controlling Fe reduction by screening the yeast ferric reductase‐deficient fre1 strain and isolated AtDTX25, a member of the Multidrug And Toxic compound Extrusion (MATE) family. AtDTX25 was shown to mediate ascorbate efflux when expressed in yeast and Xenopus oocytes, in a pH‐dependent manner. In planta, AtDTX25 is highly expressed during germination and encodes a vacuolar membrane protein. Isolated vacuoles from AtDTX25‐1 knockout mutant contained less ascorbate and more Fe than wild‐type (WT), and mutant seedlings were highly sensitive to Fe deficiency. Iron imaging further showed that the remobilisation of Fe from vacuoles was highly impaired in mutant seedlings. Taken together, our results established AtDTX25 as a vacuolar ascorbate transporter, required during germination to promote the reduction of the pool of stored Fe3+ and its remobilisation to feed the developing seedling.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17526</identifier><identifier>PMID: 34080200</identifier><language>eng</language><publisher>Lancaster: Wiley Subscription Services, Inc</publisher><subject>Animal embryos ; Arabidopsis ; ascorbate ; Ascorbic acid ; Efflux ; Embryos ; Extrusion ; Gametocytes ; Germination ; Iron ; Iron deficiency ; Life Sciences ; MATE transporter ; Membrane proteins ; Membranes ; Mutants ; Nutrient deficiency ; Oocytes ; Oxidoreductions ; Redox properties ; Reductases ; Reduction ; Seedlings ; Seeds ; Transport ; vacuole ; Vacuoles ; Vegetal Biology ; Yeast ; Yeasts</subject><ispartof>The New phytologist, 2021-09, Vol.231 (5), p.1956-1967</ispartof><rights>2021 The Authors © 2021 New Phytologist Foundation</rights><rights>Copyright © 2021 New Phytologist Trust</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3996-b3900d6d3e4469741ca2e864899494bb036df12fc999f34cce1ec5f7a5c7ba003</citedby><cites>FETCH-LOGICAL-c3996-b3900d6d3e4469741ca2e864899494bb036df12fc999f34cce1ec5f7a5c7ba003</cites><orcidid>0000-0001-5413-7844 ; 0000-0002-8884-1175 ; 0000-0001-7040-8253 ; 0000-0003-3296-5029 ; 0000-0002-5738-6712</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.17526$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.17526$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://hal.inrae.fr/hal-03258348$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Hoang, Minh Thi Thanh</creatorcontrib><creatorcontrib>Almeida, Diego</creatorcontrib><creatorcontrib>Chay, Sandrine</creatorcontrib><creatorcontrib>Alcon, Carine</creatorcontrib><creatorcontrib>Corratge‐Faillie, Claire</creatorcontrib><creatorcontrib>Curie, Catherine</creatorcontrib><creatorcontrib>Mari, Stephane</creatorcontrib><title>AtDTX25, a member of the multidrug and toxic compound extrusion family, is a vacuolar ascorbate transporter that controls intracellular iron cycling in Arabidopsis</title><title>The New phytologist</title><description>Summary Iron (Fe) is an essential element, its transport is regulated by the cell redox balance. In seeds, Fe enters the embryo as Fe2+ and is stored in vacuoles as Fe3+. Through its ferric reduction activity, ascorbate plays a major role in Fe redox state and therefore Fe transport within the seed. We searched for ascorbate membrane transporters responsible for controlling Fe reduction by screening the yeast ferric reductase‐deficient fre1 strain and isolated AtDTX25, a member of the Multidrug And Toxic compound Extrusion (MATE) family. AtDTX25 was shown to mediate ascorbate efflux when expressed in yeast and Xenopus oocytes, in a pH‐dependent manner. In planta, AtDTX25 is highly expressed during germination and encodes a vacuolar membrane protein. Isolated vacuoles from AtDTX25‐1 knockout mutant contained less ascorbate and more Fe than wild‐type (WT), and mutant seedlings were highly sensitive to Fe deficiency. Iron imaging further showed that the remobilisation of Fe from vacuoles was highly impaired in mutant seedlings. 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subjects Animal embryos
Arabidopsis
ascorbate
Ascorbic acid
Efflux
Embryos
Extrusion
Gametocytes
Germination
Iron
Iron deficiency
Life Sciences
MATE transporter
Membrane proteins
Membranes
Mutants
Nutrient deficiency
Oocytes
Oxidoreductions
Redox properties
Reductases
Reduction
Seedlings
Seeds
Transport
vacuole
Vacuoles
Vegetal Biology
Yeast
Yeasts
title AtDTX25, a member of the multidrug and toxic compound extrusion family, is a vacuolar ascorbate transporter that controls intracellular iron cycling in Arabidopsis
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