Mineral nutrition and oxidative stress

Group leader : Christian Dubos
Senior Scientist INRA
Phone : +33 4 99 61 28 18
Mail : christian.dubos@inra.fr

 

Key words

Iron, Plants, Transcription, Coumarins, Fe-S clusters, Redox

Presentation

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 [1]. 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 [2]. 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 [3]. 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 [4]. 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.

 

Team members

Permanent staff

Christian Dubos
Group leader
Research Director
INRA

Frédéric Gaymard
Research Director
INRA

Ester Izquierdo Alegre
Research Associate
INRA

Florence Vignols
Research Associate
CNRS

Nathalie Berger
Engineer
INRA

Brigitte Touraine
Engineer
INRA


Non-permanent staff

Linda Boufeldja
PhD Student
UM

Fei Gao
PhD Student

Kevin Robe
PhD Student

Dennis Brandt
Student
INRA

Main results

– 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).
– 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 a collaborative research dedicated to the characterization of the protein network involved in the scaffolding, transport and delivery of iron-sulphur (Fe-S) clusters to apo-proteins within dedicated plastidial and mitochondrial machineries. Since this date, we have demonstrated the role of several Fe-S proteins in the redox regulation of key Fe-S shuttle proteins in both compartments, involved in sulfate assimilation and in the constitution and functionality of the plastidial Photosystem I.

Significant publications

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

Collaborations

Geneviève CONEJERO, INRA Montpellier, B&PMP
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
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

Funding
Logo Labex Investissement d avenirINRAInstitut Carnot
  • I-SITE MUSE, Project: eCO2THREATS (2019-2022)
  • ANR, Project: MOBIFER (2018-2021)
  • ANR, PIA, Labex Agro, Project: FACCE (ANR-10-LABX-001-01) (2017-2018)
  • INRA BAP department, Project: MULTICSTRESS (2017-2018)
  • Institut Carnot Plant2Pro, INRA, Project: POSITIF (2018-2020)
Former team members

Permanent staff
JossiaBOUCHEREZ (TR, INRA)
Jean-François BRIAT (DR, CNRS)
Françoise CELLIER (CR, INRA)
Pierre FOURCROY (CR, CNRS)
Frédéric SANCHEZ (TR, INRA)
Tou Cheu XIONG (CR, INRA)

Students
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)

Contractual staff
Mathilde BETTEMBOURG (2017-2018), ATER UM
Cyril MAGNO (2013-2015), CDD IE
Karl RAVET (2014), Postdoc

Visiting scientists
Hannetz ROSCHZTTARDTZ (2018), 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)

Thesis defended by Nicolas Tissot

Dec. 6, 2016 – Study of gene networks involved in the regulation of iron homeostasis in Arabidopsis thaliana

Thesis defended by Guilhem Reyt

Dec. 9, 2013 – Regulation and function of ferritins in Arabidopsis thaliana : involvment in root development