Mineral nutrition and oxidative stress
Group leader: Christian Dubos
INRAE Research Director
Iron, Plants, Transcription, Coumarins, Fe-S clusters, Redox
Due to their sessile life mode, plants must face and adapt to a variety of biotic and abiotic stresses throughout their life cycle. Understanding the molecular and physiological mechanisms that modulate crop productivity under adverse environmental conditions is a major challenge for the agriculture of tomorrow. Such knowledge would be of great importance to develop strategies aiming at maintaining productivity using fewer inputs or at developing crop farming in unfavourable areas. These issues are at the heart of our research activities that focus on the control of iron (Fe) homeostasis in plants as well as on the characterization of the mechanisms involved in its assimilation.
Iron is the micronutrient that is the most often deficient in human diet, as more than 2 billion people worldwide suffer from anaemia . It is predicted that such nutritional deficiency might be reinforced at the scale of the planet in response to climate changes. For instance, it has been shown that iron level (and other major micronutrients) in most edible plant species decreases while atmospheric CO2 concentration increases . Thus, maintaining, or even improving, the ability of plants to absorb and store iron without the use of exogenous fertilizers would ensure a balanced, safer diet for a worldwide growing population facing severe climate changes. This is even more important since all iron stocks available in human food come directly or indirectly (animal sources) from plants. The entry of iron into the food chain is therefore an important question of public health that cannot be solved without a precise understanding of the molecular mechanisms that control iron homeostasis in plants as well as the assimilation of this micronutrient.
Iron is also an essential micronutrient for plant growth and development. Iron acts as a co-factor in many biological processes involving electron transfer such as photosynthesis, respiration, DNA synthesis or the assimilation of nitrogen and sulphur. The availability of this micronutrient in soils has a direct influence on the productivity of crop species, as well as on the quality of their by-products . Although iron is one of the most abundant elements in soils, it is generally poorly available to plants because it is mainly present in the form of insoluble chelates. This is the case, for example, in calcareous soils that account for one third of the world’s cultivated lands. As a consequence, plants growing on these soils suffer from iron deficiency that can affect their survival. On the other hand, iron is potentially toxic because of its ability to produce hydroxyl radicals in the presence of oxygen, generating harmful oxidative stresses to plants. Iron toxicity is mainly found in acidic or anoxic soils where its reduced form (Fe2+), which is easily assimilated by the plants, is the most prevalent. Similarly to iron deficiency, iron excess leads to severe growth defects and yield decrease . In order to avoid any iron deficiency or excess that could be detrimental to the metabolism, plants have developed a set of finely tuned molecular mechanisms involved in the acquisition, assimilation and storage of this micronutrient.
Researches conducted in our team aim at:
– Characterizing the molecular mechanisms involved in the control of iron homeostasis in plants (particularly at both transcriptional and post-translational levels).
– Studying the dynamics of coumarin secretion by plant roots in the soil to improve iron nutrition.
– Characterizing the machineries leading to Fe-S cluster assembly in chloroplasts and mitochondria, which are crucial for iron assimilation.
-  FAO, http://www.fao.org/docrep/008/w0078f/w0078f0h.htm
-  Myers et al, (2014) Nature 510:139-142
-  Briat et al. (2015) Trends Plant Sci 20:33-40.
-  Wu et al. (2014) Rice 7:8
– In recent years we have characterized target genes whose expression is activated in response to an excess of iron and in particular the genes that encode ferritins; proteins involved in the transient storage of iron (4 genes in Arabidopsis thaliana). We have identified and characterized key molecular and cellular elements that control the expression of ferritins (particularly AtFER1), both at the transcriptional and the post-transcriptional levels, in response to various stress conditions (i.e. iron excess, phosphate deficiency, drought stress, diurnal/circadian cycle, pro-oxidant treatments).
– Recently, we have been studying the transcriptional mechanisms that control iron homeostasis in plants. For instance we have shown that the transcription factor bHLH105 (known as ILR3) play a key role in the control of iron homeostasis in Arabidopsis by acting as an activator of the plant responses to iron deficiency and as a repressor of the plant responses to iron excess. In addition, we have also demonstrated that bHLH121 (also named URI) together with ILR3 and its closet homologues regulate iron homeostasis. In this later study we have shown that bHLH121 acts as a direct transcriptional activator of key genes involved in the Fe regulatory network, including bHLH38, bHLH39, bHLH100, bHLH101, PYE, BTS, BTSL1, MYB10, MYB72 as well as IMA1 and IMA2.
– We have recently characterized a new mechanism involved in plant response to iron deficiency based on coumarin secretion (secondary metabolites derived from the phenylpropanoid pathway). We have shown that the role of coumarins is to facilitate the solubilisation of the iron present in the medium prior its reduction by the ferric reductase FRO2 and its transport across the rhizodermis by the high affinity iron transporter IRT1. We have also demonstrated that coumarin secretion into the rhizosphere in response to iron deficiency is dependent on the PDR9/ABCG37 transporter activity.
– Since 2011, we perform collaborative research dedicated to the characterization of the protein network involved in the delivery of iron-sulphur (Fe-S) clusters to apo-proteins in plastids. In particular, we have characterized a family of plastid shuttle proteins (NFUs) and showed that the three NFU isoforms share common client proteins but also show specific characteristics. In addition, we have shown that these NFU proteins are involved in the assimilation of sulfate, the constitution of photosystem I and in the biosynthesis of branched chain amino acids.
Gao F✉, Dubos C✉ (2020) Transcriptional integration of the plant responses to iron availability. J. Exp. Bot., (accepted)
Robe K, Izquierdo E, Vignols F, Rouached H, Dubos C✉ (2021) The Coumarins: Secondary metabolites playing a primary role in plant nutrition and health. Trends Plant Sci., (in press)
Robe K, Conéjéro G, Gao F, Lefebvre-Legendre L, Sylvestre-Gonon E, Rofidal V, Hem S, Rouhier N, Barberon M, Hecker A, Gaymard F, Izquierdo E✉, Dubos C✉ (2020) Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process. New Phytol., (accepted)
Berger N, Vignols F, Touraine B, Taupin-Broggini M, Rofidal V, Demolombe V, Santoni V, Rouhier N, Gaymard F, Dubos C✉ (2020) A global proteomic approach sheds new light on potential iron-sulfur client proteins of the chloroplastic maturation factor NFU3. Int. J. Mol. Sci., 21(21):8121
Gao F, Robe K, Dubos C✉ (2020) Further insights into the role of bHLH121 in the regulation of iron homeostasis in Arabidopsis thaliana. Plant Signal. Behav., 15(10):1795582
Robe K*, Gao F*, Bonillo P, Tissot N, Gaymard F, Fourcroy P, Izquierdo E, Dubos C✉ (2020) Sulphur availability modulates Arabidopsis thaliana responses to iron deficiency. PLoS one, 15(8): e0237998
Berger N, Vignols F, Przybyla-Toscano J, Roland M, Rofidal V, Touraine B, Zienkiewicz K, Couturier J, Feussner I, Santoni V, Rouhier N, Gaymard F, Dubos C✉ (2020) Identification of client iron-sulfur proteins of the chloroplastic NFU2 transfer protein in Arabidopsis thaliana. J. Exp. Bot., 71(14):4171-4187
Roschzttardtz H✉, Gaymard F, Dubos C (2020) Transcriptional regulation of iron distribution in seeds: A perspective. Front. Plant Sci., 11:725
Roland M, Przybyla-Toscano J*, Vignols F*, Berger N*, Azam T, Christ L, Santoni V, Wu H-C, Dhalleine T, Johnson MK, Dubos C, Couturier J, Rouhier N✉ (2020) The plastidial Arabidopsis thaliana NFU1 protein binds and delivers [4Fe-4S] clusters to specific client proteins. J. Biol. Chem., 295(6): 1727-1742
Gao F, Robe K, Bettembourg M, Navarro N, Rofidal V, Santoni V, Gaymard F, Vignols F, Roschzttardtz H, Izquierdo E, Dubos C✉ (2019) The transcription factor bHLH121 interacts with bHLH105 (ILR3) and its closest homologs to regulate iron homeostasis in Arabidopsis. Plant Cell, (in press)
Rey P, Taupin-Broggini M, Couturier J, Vignols F, Rouhier N (2019) Is there a role for glutaredoxins and BOLAs in the perception of the cellular iron status in plants? Front. Plant Sci. 10:712
Tissot N, Robe K*, Gao F*, Grant-Grant S, Boucherez J, Bellegarde F, Maghiaoui A, Marcelin R, Izquierdo E, Benhamed M, Martin A, Vignols F, Roschzttardtz H, Gaymard F, Briat J-F, Dubos C (2019) Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3. New Phytol., (accepted)
Gao F*, Robe K*, Gaymard F, Izquierdo E, Dubos C (2019) The transcriptional control of iron homeostasis in plants: A tale of bHLH transcription factors?. Front. Plant Sci., 10:6
Touraine B, Vignols F*, Przybyla-Toscano J*, Ischebeck T, Dhalleine T, Wu H-C, Magno C, Berger N, Couturier J, Dubos C, Feussner I, Caffarri S, Havaux M, Rouhier N, Gaymard F (2019) Iron–sulfur protein NFU2 is required for branched-chain amino acid synthesis in Arabidopsis roots. J. Exp. Bot., 70(6):1875-1889
Pal S*, Kisko M*, Dubos C, Lacombe B, Berthomieu P, Krouk G✉, Rouached H✉ (2017) TransDetect identifies a new regulatory module controlling phosphate accumulation. Plant Physiol., 175(2):916-926
Kelemen Z, Przybyla-Toscano J, Tissot N, Lepiniec L, Dubos C✉ (2016) Plant Synthetic Promoters – Fast and efficient cloning of cis-regulatory sequences for high-throughput yeast one-hybrid analyses of transcription factors. Methods Mol. Biol., 1482:139-149
Xiong TC✉, Sanchez F, Briat J-F, Gaymard F, Dubos C (2016) Plant Synthetic Promoters – Spatio-temporal imaging of promoter activity in intact plant tissues. Methods Mol. Biol., 1482:103-110
Sisó-Terraza P*, Luis-Villarroya A*, Fourcroy P, Briat J-F, Abadía A, Gaymard F, Abadía J, Álvarez-Fernández A✉ (2016) Accumulation and secretion of coumarinolignans and other coumarins in Arabidopsis thaliana roots in response to iron deficiency at high pH. Front. Plant Sci., 7:1711
Fourcroy P*, Tissot N*, Gaymard F, Briat J-F, Dubos C✉ (2016) Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1 / FRO2 high affinity root Fe2+ transport system. Mol. Plant, 9(3):485-488
Knuesting J, Riondet C, Maria C, Kruse I, Bécuwe N, König N, Berndt C, Tourrette S, Guilleminot-Montoya J, Herrero E, Gaymard F, Balk J, Belli G, Scheibe R, Reichheld J-P, Rouhier N, Rey P✉ (2015) Arabidopsis glutaredoxin S17 and its partner, the nuclear factor Y subunit C11/negative cofactor 2α, contribute to maintenance of the shoot apical meristem under long-day photoperiod. Plant Physiol., 167(4):1643-1658
Briat J-F✉, Rouached H, Tissot N, Gaymard F, Dubos C (2015) Integration of P, S, Fe and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front. Plant Sci., 6:290
Reyt G, Boudouf S, Boucherez J, Gaymard F, Briat J-F✉ (2015) Iron and ferritin dependent ROS distribution impact Arabidopsis root system architecture. Mol. Plant, 8(3):439-453
Briat J-F✉, Dubos C, Gaymard F (2015) Iron nutrition, biomass production and plant product quality. Trends Plant Sci., 20(1):33-40
Tissot N, Przybyla-Toscano J, Reyt G, Castel B, Duc C, Boucherez J, Gaymard F, Briat J-F✉, Dubos C✉ (2014) Iron around the clock. Plant Sci., 224:112-119
Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadía J, Álvarez-Fernández A, Briat J-F✉ (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol., 201(1):155-167
Couturier J*, Wu H-C*, Dhalleine T, Pégeot H, Sudre D, Gualberto J, Jacquot J-P, Gaymard F, Vignols F, Rouhier N✉ (2014) Monothiol glutaredoxin-BolA interactions: redox control of Arabidopsis thaliana BolA2 and SufE1. Mol. Plant, 7(1):187-205
Koen E, Besson-Bard A, Duc C, Astier J, Gravot A, Richaud P, Lamotte O, Boucherez J, Gaymard F, Wendehenne D (2013) Arabidopsis thaliana nicotianamine synthase 4 is required for proper response to iron deficiency and to cadmium exposure. Plant Sci., 209:1-11
Gao H, Subramanian S, Couturier J, Naik SG, Kim S-K, Leustek T, Knaff DB, Wu H-C, Vignols F, Huynh BH, Rouhier N, Johnson MK✉ (2013) Arabidopsis thaliana Nfu2 Accommodates [2Fe-2S] or [4Fe-4S] Clusters and Is Competent for in Vitro Maturation of Chloroplast [2Fe-2S] and [4Fe-4S] Cluster-Containing Proteins. Biochemistry-US, 52(38):6633-6645
Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E, Briat J-F, Gaymard F✉ (2013) Arabidopsis FERRITIN 1 (AtFer1) gene regulation by the PHOSPHATE STARVATION RESPONSE 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. J. Biol. Chem., 288(31):22670-22680
Sudre D*, Gutierrez-Carbonell E*, Lattanzio G, Rellán-Álvarez R, Gaymard F, Wohlgemuth G, Fiehn O, Álvarez-Fernández A, Zamarreño AM, Bacaicoa E, Duy D, García-Mina JM, Abadía J, Philippar K, López-Millán A-F, Briat J-F (2013) Iron-dependent modifications of the flower transcriptome, proteome, metabolome and hormonal content in an Arabidopsis ferritin mutant. J. Exp. Bot., 64(10):2665-2688
Couturier J, Touraine B, Briat J-F, Gaymard F, Rouhier N (2013) The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions. Front. Plant Sci., 4:259
Gabriel KROUK, INRA Montpellier, B&PMP
Antoine MARTIN, INRA Montpellier, B&PMP
Hatem ROUACHED, INRA Montpellier, B&PMP
Moussa BENHAMED, University of Paris-Sud, IPS2
Mathilde CAUSSE, INRA Avignon, GAFL
Joseph CHAMIEH, University of Montpellier, IBMM
Hélène DEMENE, CNRS Montpellier, CBS
Pascal REY, CEA Cadarache, BIAM
Jean-Philippe REICHHELD, CNRS Perpignan, LGDP
Christophe ROTHAN, INRA Bordeaux, BFP
Nicolas ROUHIER, University of Lorraine, IAM
Sébastien THOMINE, CNRS Gif, I2BC
Janneke BALK, England, University of Cambridge
Ivo FEUSSNER, Germany, University of Göttingen
Michael K. JOHNSON, USA, University of Georgia
Hannetz ROSCHZTTARDTZ, Chile, Pontifical Catholic University of Chile
Hui-Chen WU, Taiwan, National University of Tainan
– Labex Agro, CALCLIM Project (2020-2022)
– i-SITE MUSE, eCO2THREATS Project (2019-2022)
– INRA département BAP, BolAFER Project (2019-2020)
– ANR, MOBIFER Project (2018-2021)
– Labex Agro, FACCE Project (2017-2018)
– INRA département BAP, MULTICSTRESS Project (2017-2018)
– Institut Carnot Plant2Pro, POSITIF Project (2018-2020)
– INRA département BAP, HARSH Project (2014-2015)
– ANR, FeS-TRAFFIC Project (2014-2017)
Former team members
Jossia BOUCHEREZ (TR, INRA)
Jean-François BRIAT (DR, CNRS)
Françoise CELLIER (CR, INRA)
Pierre FOURCROY (CR, CNRS)
Frédéric GAYMARD (DR, INRA)
Frédéric SANCHEZ (TR, INRA)
Tou Cheu XIONG (CR, INRA)
Dennis BRANDT (2019), ERASMUS (Münster, Germany)
Julie GUERREIRO (2019), L3 (Montpellier)
Maël TAUPIN-BROGGINI (2018), M2 (Montpellier)
Mélusine SENANAYAKE (2018), L3 (Montpellier)
Thomas FERRAN (2018), BTS (Montpellier)
Chafika ABDOU ISSA (2017), M1 (Nantes)
Pauline DUVAL (2017), L3 (Montpellier)
Vincent OGLIENGO (2017), L3 (Montpellier)
Guillaume PERBECH (2017), L3 (Montpellier)
Kevin ROBE (2017), M2 / VetAgro (Clermont-Ferrand)
Pauline BONILLO (2016), M1 (Montpellier)
Jennifer BORN (2016), L3 ERASMUS (Göttingen, Germany)
Nicolas DURA (2016), BTS (Montpellier)
Thi Hong Ha NGUYEN (2016), L3 (Hanoï, Viêt Nam)
Amel MAGHIAOUI (2015), L3 Pro (Toulouse)
Laura MARTINS (2015), M2 (Montpellier)
Caroline SCIALLANO (2015), L3 (Lyon)
Soukaina BOUDOUF (2014), M1 (Montpellier)
Romain MARCELIN (2014), L3 (Montpellier)
Baptiste CASTEL (2013), M1 (Montpellier)
Cyril MAGNO (2013), M2 (Montpellier)
Benoit MERMAZ (2013), L3 (Montpellier)
Jonathan PRZYBYLA-TOSCANO (2013), M2 (Montpellier)
Nicolas TISSOT (2013-2016), Doctorant (Montpellier)
Mathilde BETTEMBOURG (2017-2018), ATER UM
Cyril MAGNO (2013-2015), CDD IE
Karl RAVET (2014), Postdoc
Susana GRANT GRANT (2019), PhD student (Pontifical Catholic University of Chile, Chile)
Hannetz ROSCHZTTARDTZ (2018, 2019), Assistant Professeur (Pontifical Catholic University of Chile, Chile)
Tamara MENDEZ CASTRO (2018), PhD student (University of Talca, Chile)
Nicolas ROUHIER (2017-2018), Professor (University of Lorraine, France)
Jonathan PRZYBYLA-TOSCANO (2017), ATER (University of Lorraine, France)
Mélanie ROLAND (2017), PhD student (University of Lorraine, France)
Patricia SISÓ-TERRAZA (2013), PhD student (CSIC, Saragosse, Spain)
Hui-Chen WU (2016, 2017), Assistant Professor (National University of Tainan, Taiwan)
The plastidial Arabidopsis thaliana NFU1 protein binds and delivers [4Fe-4S] clusters to specific client proteins
Some news on the iron–sulfur biogenesis and the role of NFU1 in this process. A manuscript in collaboration with Nicolas Rouhier’s team and issued from Mélanie’s PhD thesis (Roland et al., 2020 – J Biol Chem).
Is There a Role for Glutaredoxins and BOLAs in the Perception of the Cellular Iron Status in Plants?
A recent review of the role of glutharedoxins and BOLA in the perception of iron status in plants (Rey et al., 2019 – Front Plant Sci).
A recent review on the role of the bHLH transcription factors (but not only) in the control of plant iron homeostasis from Fei and Kevin (Gao et Robe et al., 2019 – Front plant Sci)
Interested in the functional, structural or biochemical characteristics of plant serinyl glutathione transferases (GST)? here is a recent review to learn all about this class of protein (Sylvestre-Gonon et al., 2019 – front Plant Sci).
Some news on the iron–sulfur biogenesis, a manuscript issued from Brigitte’s work (Touraine et al, 2019 – J Exp Bot).
The Transcription Factor bHLH121 Interacts with bHLH105 (ILR3) and its Closest Homologs to Regulate Iron Homeostasis in Arabidopsis
bHLH121 a key gene for the control of iron homeostasis in Arabidopsis (Gao et al., 2019 – Plant Cell).