Metal Mobility (Memo)

Group leader: Catherine Curie
Research Director CNRS

 

 

 Key words

Transport, Iron, Manganese, Arabidopsis, Regulation, Membrane trafficking

Presentation

Our team studies the molecular bases of iron (Fe) and manganese (Mn) homeostases in the flower plant Arabidopsis thaliana and the moss Physcomitrella patens.

Fe and Mn play a crucial role in cell life as cofactors of numerous enzymes that control key metabolisms such as photosynthesis, respiration or nucleic acids biosynthesis. However, despite their high abundance in the Earth crust, their low solubility in soils limits their bioavailability in a majority of cultivated lands in the planet.

Our objective is to understand the mechanisms by which plants cope with these environmental constraints. To that aim, we focus on the identification of membrane transporters of Fe and/or Mn and their regulators in Arabidopsis thaliana and Physcomitrella patens. Furthermore, Fe mobility is tightly linked to its redox state (Fe2+ or Fe3+) as well as to the nature of the complex that it forms with a set of ligands. Indeed, in order to cross the membrane, each redox/ligand combination must recruit a specific transporter. We are therefore also looking for actors controlling this so-called “Fe speciation”: oxidases and reductases, Fe ligands and their membrane transporters.

To nail down candidate genes and characterize their function, we combine reverse and quantitative (QTL, GWAS) genetics with biochemistry/analytical chemistry and cell biology.

Our team has a strong expertise in the utilization and development of imaging tools enabling to visualize 1) cellular Fe (Perls-DAB histochemistry) and 2) calcium waves that are produced in response to the plant’s Fe or Mn status.

In addition, a last generation atomic spectrometer (MP-AES) based in the team (https://www1.montpellier.inra.fr/wp-inra/bpmp/en/platform/multi-elemental-analyses-service/) allows to perform sensitive and high-throughput multielemental analyses of plant samples (mutants, natural variants) in response to metallic treatments (deficiency or excess).

Team members
Main results
Iron imaging method. Thanks to the implementation of a simple method to image Fe at the subcellular level, we have been able to localize the main pools of Fe throughout the plant organs (Rozschttardtz et al., 2009, 2011a). This powerful method has also enabled us to tackle the function of transporters of either Fe or ligands of Fe in Arabidopsis.

NRAMP1 functions in Mn acquisition by Arabidopsis. In very low Mn conditions, plants synthesize NRAMP1, a member of the widely conserved divalent metal transporters, which takes up Mn at the root surface. In the absence of a functional NRAMP1 gene, growth of Arabidopsis plants upon Mn deficiency is impaired (Cailliatte et al., 2010).

Role of citrate in the apoplastic transport of iron. The Fe-citrate complex is stable in xylem sap and apoplastic spaces. We have shown that the citrate effluxer FRD3 contributes to Fe movement between non-symplastically connected tissues by solubilizing Fe between the cells (Rozschttardtz et al., 2011b). Fe nutrition of the pollen grain thus depends on Fe-citrate availability in the anther locule.

Fe nutrition of the embryo relies on ascorbate-mediated reduction of FeIII. During embryogenesis, we have shown that the Arabidopsis embryo releases ascorbate to enable FeIII reduction and subsequent FeII uptake (Grillet et al., 2014).

Figure: Schematic representation of ascorbate-dependent Fe influx into the embryo. The Arabidopsis embryo was stained with Perls-DAB to show Fe accumulation into the vasculature.

 

 

NRAMP2 transporter distributes Mn to organelles. We have shown that NRAMP2 is a resident protein of the Trans-Golgi network, which is required for proper allocation of Mn into vacuole and chloroplasts, photosynthesis activity and cellular redox balance (Alejandro et al., 2017).

Significant publications

Thibault Kosuth(d), Alexandra Leskova, Reyes Ródenas, Grégory Vert, Catherine Curie, Loren Castaings (Aug 2023) Phosphorylation by CIPK23 regulates the high-affinity Mn transporter NRAMP1 in Arabidopsis. Febs Lett. 597(16):2048-2058

Kosuth T, Leskova A, Castaings L, Curie C (2023) Golgi in and out: multifaceted role and journey of manganese. New Phytol., 238(5):1795-1800

Alcon C, Xiong TC (2023) Calcium live imaging at multi-scales from cellular to organ level in Arabidopsis thaliana. in Ivan Couée (Eds): Plant Abiotic Stress Signaling. Methods Mol. Biol., 2642:85-95

Brun A, Smokvarska M, Wei L, Chay S, Curie C, Mari S (2022) MCO1 and MCO3, two putative ascorbate oxidases with ferroxidase activity, new candidates for the regulation of apoplastic iron excess in Arabidopsis. Plant Direct, 6(11):e463

Grant-Grant S, Schaffhauser M, Baeza-González PA, Gao F, Conéjéro G, Gaymard F, Dubos C, Curie C, Roschzttardtz H (2022) B3 transcription factors determine iron distribution and FERRITIN gene expression in embryo but do not control total seed iron content. Front. Plant Sci., (accepted)

Kechid M, Desbrosses G, Gamet L, Castaings L, Varoquaux F, Djekoun A, Touraine B (2022) Arabidopsis growth-promotion and root architecture responses to the beneficial rhizobacterium Phyllobacterium brassicacearum strain STM196 are independent of the nitrate assimilatory pathway. Plants-Basel, 11(1):128

Then C*, Bellegarde F*, Schivre G*, Martinière A, Macia J-L, Xiong TC, Drucker M (2021) Plant viruses can alter aphid-triggered calcium elevations in infected leaves. Cells, 10(12):3534

Hoang MTT, Almeida DM, Chay S, Alcon C, Corratgé-Faillie C, Curie C, Mari S (2021) AtDTX25, a member of the multidrug and toxic compound extrusion family, is a vacuolar ascorbate transporter that controls intracellular iron cycling in Arabidopsis. New Phytol., 231(5):1956-1967

Castaings L, Alcon C, Kosuth T, Correia D, Curie C (2021) Manganese triggers phosphorylation-mediated endocytosis of the Arabidopsis metal transporter NRAMP1. Plant J., 106(5):1328-1337

Alejandro S, Cailliatte R, Alcon C, Dirick L, Domergue F, Correia D, Castaings L, Briat J-F, Mari S, Curie C (2017) Intracellular distribution of manganese by the trans-golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. Plant Cell, 29(12):3068-3084

Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci. Rep.-UK, 6:37222

Grillet L*, Ouerdane L*, Flis P, Hoang MTT, Isaure M-P, Lobinski R, Curie C, Mari S (2014) Ascorbate efflux as a new strategy for iron reduction and transport in plants. J. Biol. Chem., 289(5):2515-2525

Divol F*, Couch D*, Conéjéro G, Roschzttardtz H, Mari S, Curie C (2013) The Arabidopsis YELLOW STRIPE LIKE 4 and 6 transporters control iron release from the chloroplast. Plant Cell, 25(3):1040-1055

Barberon M*, Zelazny E*, Robert S, Conéjéro G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants. P. Natl. Acad. Sci. USA, 108(32):E450-E458

Roschzttardtz H, Grillet L, Isaure M-P, Conéjéro G, Ortega R, Curie C, Mari S (2011) Plant cell nucleolus as a hot spot for iron. J. Biol. Chem., 286(32):27863-27866

Roschzttardtz H*, Séguéla-Arnaud M*, Briat J-F, Vert G, Curie C (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell, 23(7):2725-2737

Sivitz A, Grinvalds C, Barberon M, Curie C, Vert G (2011) Proteasome-mediated turnover of the transcriptional activator FIT is required for plant iron deficiency responses. Plant J., 66(6):1044-1052

Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the Metal Transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell, 22(3):904-917

Roschzttardtz H, Conéjéro G, Curie C, Mari S (2009) Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol., 151(3):1329-1338

Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot.-London, 103(1):1-11

Séguéla M, Briat J-F, Vert G, Curie C (2008) Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J., 55(2):289-300

Briat J-F, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants. Curr. Opin. Plant Biol., 10(3):276-282

Le Jean M, Schikora A, Mari S, Briat J-F, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotiananmine seed loading. Plant J., 44(5):769-782

Vert G, Briat J-F, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root Iron uptake system by local and long-distance signals. Plant Physiol., 132(2):796-804

Curie C, Briat J-F (2003) Iron transport and signaling in plants. Annu. Rev. Plant Phys., 54:183-206

Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell, 14(6):1223-1233

Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat J-F, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature, 409(6818):346-349

 

Collaborations
  • French collaborations:

Sébastien Thomine, I2BC (Gif-sur-Yvette)

Julio Saez-Vasquez (Université Perpignan)

Christophe Bailly, IBPS (Université Pierre et Marie Curie)

Marie-Pierre Isaure LCABIE (Université Pau)

Karine Gallardo (INRA Dijon)

Frédéric Domergue (INRA Bordeaux)

  • International collaborations:

Wolfgang Schmidt, Academia Sinica (Taipei, Taiwan)

Lola Penarrubia (University Valencia, Spain)

Alessandro Alboresi, Department Biology (Université Padoue, Italie)

Funding
  • Project ANR CIDS (2006-2009)
  • Project ANR DISTRIMET (2007-2010)
  • Project ANR HEMOLI (2007-2010)
  • Project ANR TRAFIRT (2008-2011)
  • Marie-Curie IEF BIOCHEMIRT. Manuel Gonzalez-Guerrero (2008-2010)
  • Project ANR PLANTMAN (2012-2015)
  • Project ANR MANOMICS (2012-2016)
  • Project ANR SUBCELIF (2014-2017)
  • Contract Agropolis Fondation-Solvay/Rhodia (2014-2015)
  • Project BAP INRA INRONSEED (2016-2017)
  • Contract Solvay/Rhodia (2016-2018)
  • Project ANR ISISTOR (2017-2020)
Former team members
Hannetz Roschzttardtz, Université pontificale du Chili hroschzttardtz@bio.puc.cl

Rémy Cailliatte, Centre INRA d’Avignon remy.cailliatte@inra.fr

Loren Castaings, Université Montpellier loren.castaings@supagro.fr

Santiago Alejandro, Université de Halle santiago.alejandro-martinez@landw.uni-halle.de

Louis Grillet, Academia sinica Taipei grillet@gate.sinica.edu.tw

CDD Role of micronutrients (Fe, Mn, Zn) in microsporogenesis. Project acronym: MICROMET Overall

CDD Role of micronutrients (Fe, Mn, Zn) in microsporogenesis. Project acronym: MICROMET Overall – Memo

Research engineer in plant experimentation and production: study of the impact of bacterial metallophores on plant metal nutrition

Research engineer in plant experimentation and production: study of the impact of bacterial metallophores on plant metal nutrition – 2 years – MEMO

IBIP seminar: Edgar Peiter

Thursday, June 22 2023 – An organellar journey – mechanisms of intracellular calcium and manganese distribution in plants and crops

IBIP seminar: Jean Colcombet

Thursday, May 30 2023 – The MKK3 module integrates nitrate and light signals to modulate secondary dormancy

Thesis defended by Thibault Kosuth

Wednesday may 31 2023- Manganese transport in Arabidopsis : post-translational regulation of the manganese transporter NRAMP1

Thesis defended by Alexis Brun

September 8, 2022 – Role of multicopper oxidases in iron homeostasis in Arabidopsis thaliana

IBIP seminar: Valèrio Giuffrida

June 9, 2022 – Learning to Count Leaves of Plants

IBIP seminar – Akihiro Saito

Nov 28, 2019 – Mitophagy and chlorophagy as an essential strategy to alleviate toxicity of heavy metals

IBIP seminar – Diego M. Almeida

Sept 20, 2018 – Regulation of the OsNHX1 Gene Expression: Identification and Characterization of Novel Transcription Factors