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
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
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)
Li L*, Zhu Z*, Liao Y*, Yang C, Fan N, Zhang J, Yamaji N, Dirick L, Ma JF, Curie C, Huang C-F✉ (2022) NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis. Plant J., (accepted)
Nguyen NT✉, Khan MA, Castro-Guerrero NA, Chia J-C, Vatamaniuk OK, Mari S, Jurisson JS, Mendoza-Cozatl DG✉ (2022) Iron availability within the leaf vasculature determines the magnitude of iron deficiency responses in source and sink tissues in Arabidopsis. Plant Cell Physiol., (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., (accepted)
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
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
