Identification of a Tri-Iron(III), Tri-Citrate Complex in the Xylem Sap of Iron-Deficient Tomato Resupplied with Iron: New Insights into Plant Iron Long-Distance Transport

Rellán‐Álvarez, Rubén; Giner-Martínez-Sierra, Justo; Orduna, Jesús; Orera, Irene; Rodríguez-Castrillón, José Ángel; García-Alonso, J. Ignacio; Abadı́a, Javier; Álvarez‐Fernández, Ana

doi:10.1093/pcp/pcp170

Cited by 240 publications

(162 citation statements)

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“…23 More interestingly, a tri-Fe(III) tricitrate complex involved in Fe transport has been recently identified in xylem sap of tomato plants 24 and our results show that Fe(III)…”

Section: Al and Fe Are Complexed By Tricitratesupporting

confidence: 64%

“…The Fe complex was modelled as having an oxobridged tri-Fe(III) (Fe 3 Ocit 3 ) core and owing to its compact molecular geometry it is expected to permeate the plasmodesmata directly. 24 The authors also reported that while both Fe 3 cit 3 and Fe 3 Ocit 3 complexes could be identified in Fe-citrate standard solutions, only Fe 3 Ocit 3 was found in xylem samples. However, the Fe 3 cit 3 complex was detected in P. almogravensis root samples and represents the first report of this complex in biological samples (Fig.…”

Section: Al and Fe Are Complexed By Tricitratementioning

confidence: 95%

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Identification of the tri-Al tricitrate complex in Plantago almogravensis by hydrophilic interaction LC with parallel ICP-MS and electrospray Orbitrap MS/MS detection

et al. 2013

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The identification of the ligands binding Al is essential to understand the mechanisms by which plants detoxify Al internally. However, studies concerning the speciation of Al have been frustrated by its complex chemistry. This work describes the identification of the tri-Al tricitrate (Al 3 cit 3 ) complex in Plantago almogravensis, encompassing an integrated mass spectrometry approach based on hydrophilic interaction liquid chromatography (HILIC) and parallel detection by ICP-MS and ESI-MS/MS. This work also reports that both Al and Fe are bound by tricitrate, sometimes simultaneously, and the consequences of this finding are discussed. Of the complexes separated by size exclusion chromatography, Al 3 cit 3 is the most stable occurring in P. almogravensis as it was the only one recovered after HILIC. This approach provided new information on the mechanism of Al detoxification in P. almogravensis, namely that Al is bound by the organic acid citrate and that the relative concentration of the detected complexes is affected by the organ type and internal Al concentration, and has potential for studying the speciation of Al in less tolerant plants.

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“…23 More interestingly, a tri-Fe(III) tricitrate complex involved in Fe transport has been recently identified in xylem sap of tomato plants 24 and our results show that Fe(III)…”

Section: Al and Fe Are Complexed By Tricitratesupporting

confidence: 64%

Section: Al and Fe Are Complexed By Tricitratementioning

confidence: 95%

Identification of the tri-Al tricitrate complex in Plantago almogravensis by hydrophilic interaction LC with parallel ICP-MS and electrospray Orbitrap MS/MS detection

et al. 2013

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“…We describe an organic-acid-mediated mechanism that starts in the root tip and adjusts the root developmental response to low Pi. Organic acids have also been implicated in Fe uptake (30) and protection of the root from the entrance of toxic Al +3 ions (22,23). Taken all together, the evidence suggests that organic-acid exudation is a critical checkpoint in plant nutrition as these molecules do not only protect the root from the entry of toxic ions and enhance nutrient uptake, but also contribute to the modifications of root development that increase the soilexploration ability of the plant to enhance nutrient uptake.…”

Section: Malate Treatment Rescued the Expression Of Local-response Genesmentioning

confidence: 99%

“…Accumulation of Fe in the apoplast of cells in the RAM is required to activate the primary root response to low Pi availability (20). As carboxylateiron complexes have been reported to participate in iron transport and acquisition in plants ( [28][29][30] and malate efflux is affected in stop1 and almt1 mutants (21,22), we explored whether malate exudation plays a role in the Fe accumulation mechanism that is required to trigger primary root growth inhibition in response to low Pi availability. First, we tested whether malate is required for the accumulation of Fe in the apoplast of RAM cells using Perlsdiaminobenzidine (DAB) histochemical Fe staining, which allows the detection of changes in labile Fe +3 (20), on the root tips of WT, stop1, and almt1 in low-Pi media with or without 1 mM malate ( Fig.…”

Section: Almt1 Is Expressed In the Ram Of Arabidopsis Under Pi-deficimentioning

confidence: 99%

Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Mora-Macías

Ojeda-Rivera

Gutiérrez-Alanís

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Low phosphate (Pi) availability constrains plant development and seed production in both natural and agricultural ecosystems. When Pi is scarce, modifications of root system architecture (RSA) enhance the soil exploration ability of the plant and lead to an increase in Pi uptake. In Arabidopsis, an iron-dependent mechanism reprograms primary root growth in response to low Pi availability. This program is activated upon contact of the root tip with low-Pi media and induces premature cell differentiation and the arrest of mitotic activity in the root apical meristem, resulting in a short-root phenotype. However, the mechanisms that regulate the primary root response to Pi-limiting conditions remain largely unknown. Here we report on the isolation and characterization of two low-Pi insensitive mutants (lpi5 and lpi6), which have a long-root phenotype when grown in low-Pi media. Cellular, genomic, and transcriptomic analysis of low-Pi insensitive mutants revealed that the genes previously shown to underlie Arabidopsis Al tolerance via root malate exudation, known as SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) and ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (ALMT1), represent a critical checkpoint in the root developmental response to Pi starvation in Arabidopsis thaliana. Our results also show that exogenous malate can rescue the long-root phenotype of lpi5 and lpi6. Malate exudation is required for the accumulation of Fe in the apoplast of meristematic cells, triggering the differentiation of meristematic cells in response to Pi deprivation.

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“…Citrate concentration is indeed markedly increased by iron starvation in xylem exudates (Brown, 1966;Ló pez-Millá n et al, 2000), and the acidic pH of this apoplastic fluid is compatible with the stability of the Fe-citrate complex. Only recently, however, has the presence of Fe-citrate complexes, in the form of tri-Fe(III) tri-citrate and di-Fe(III) dicitrate, been detected in xylem exudates of tomato plants (Rellá n-Alvarez et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

The FRD3 Citrate Effluxer Promotes Iron Nutrition between Symplastically Disconnected Tissues throughout Arabidopsis Development

et al. 2011

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We present data supporting a general role for FERRIC REDICTASE DEFECTIVE3 (FRD3), an efflux transporter of the efficient iron chelator citrate, in maintaining iron homeostasis throughout plant development. In addition to its well-known expression in root, we show that FRD3 is strongly expressed in Arabidopsis thaliana seed and flower. Consistently, frd3 lossof-function mutants are defective in early germination and are almost completely sterile, both defects being rescued by iron and/or citrate supply. The frd3 fertility defect is caused by pollen abortion and is associated with the male gametophytic expression of FRD3. Iron imaging shows the presence of important deposits of iron on the surface of aborted pollen grains. This points to a role for FRD3 and citrate in proper iron nutrition of embryo and pollen. Based on the findings that iron acquisition in embryo, leaf, and pollen depends on FRD3, we propose that FRD3 mediated-citrate release in the apoplastic space represents an important process by which efficient iron nutrition is achieved between adjacent tissues lacking symplastic connections. These results reveal a physiological role for citrate in the apoplastic transport of iron throughout development, and provide a general model for multicellular organisms in the cell-to-cell transport of iron involving extracellular circulation.

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Identification of a Tri-Iron(III), Tri-Citrate Complex in the Xylem Sap of Iron-Deficient Tomato Resupplied with Iron: New Insights into Plant Iron Long-Distance Transport

Cited by 240 publications

References 54 publications

Identification of the tri-Al tricitrate complex in Plantago almogravensis by hydrophilic interaction LC with parallel ICP-MS and electrospray Orbitrap MS/MS detection

Identification of the tri-Al tricitrate complex in Plantago almogravensis by hydrophilic interaction LC with parallel ICP-MS and electrospray Orbitrap MS/MS detection

Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

The FRD3 Citrate Effluxer Promotes Iron Nutrition between Symplastically Disconnected Tissues throughout Arabidopsis Development

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