Mineral nutrition and oxidative stress

Group leader: Christian Dubos
INRAE Research Director

 

 

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 about 1 billion people worldwide suffer from iron deficiency anaemia (IDA) [1]. It is predicted that climate changes might reinforced such nutritional deficiency at the global scale. 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 oxides and hydroxides. 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. Such as 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 and to precisely depict the function of these molecules in this process.
– Characterizing the machineries leading to iron-sulphur (Fe-S) cluster assembly in chloroplasts and mitochondria, which are crucial for iron assimilation.

 

Team members
Main results

– Our previous work on the study of the plant response to iron excess (using as marker gene the ferritins, which encode proteins involved in the transient storage of iron) lead us to study 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, in part, 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. More recently, we have shown that the accumulation and transport of these metabolites are complex and dynamic mechanisms.
– We have contributed 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.

Significant publications

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✉ (2021) Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process. New Phytol., 229(4):2062-2079

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

Sylvestre-Gonon E, Law S, Schwartz M, Robe K, Keech O, Didierjean C, Dubos C, Rouhier N✉, Hecker A✉ (2019) Functional, structural and biochemical features of plant serinyl-glutathione transferases. Front. Plant Sci., 10:608

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
Hélène DEMENE, CNRS Montpellier, CBS
Jean-Philippe REICHHELD, CNRS Perpignan, LGDP
Pascal REY, CEA Cadarache, BIAM
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
Mitsunori SEO, Japan, RIKEN
Hui-Chen WU, Taiwan, National University of Tainan

Funding
Logo Labex Investissement d avenirINRAInstitut Carnot

 

 

– Marie Skłodowska-Curie Actions, PLANTSEEFE Project (2021-2023)
– BioCampus, PEPIRON Project (2021)
– Labex Agro, CALCLIM Project (2020-2022)
– i-SITE MUSE, eCO2THREATS Project (2019-2021)
– 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
Permanent staff
Jossia BOUCHEREZ (TR, INRAE)
Jean-François BRIAT (DR, CNRS)
Françoise CELLIER (CR, INRAE)
Pierre FOURCROY (CR, CNRS)
Frédéric GAYMARD (DR, INRAE)
Frédéric SANCHEZ (TR, INRAE)
Tou Cheu XIONG (CR, INRAE)

Students
Victorine NOËL, (2020), L3 (Montpellier)
Mélia PETIT-BECMONT (2020), L3 (Montpellier)
Dennis BRANDT (2019), ERASMUS (Münster, Germany)
Julie GUERREIRO (2019), L3 (Montpellier)
Thomas FERRAN (2018), BTS (Montpellier)
Kevin ROBE (2018-2021), Doctorant (Montpellier)
Mélusine SENANAYAKE (2018), L3 (Montpellier)
Maël TAUPIN-BROGGINI (2018), M2 (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
Karl RAVET (2014), Postdoc
Cyril MAGNO (2013-2015), CDD IE

Visiting scientists
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)
Jonathan PRZYBYLA-TOSCANO (2017), ATER (University of Lorraine, France)
Mélanie ROLAND (2017), PhD student (University of Lorraine, France)
Nicolas ROUHIER (2017-2018), Professeur (Université de Lorraine)
Hui-Chen WU (2016-2017), Assistant Professeur (Université nationale de Tainan, Taïwan)
Patricia SISÓ-TERRAZA (2013), Doctorante (CSIC, Saragosse, Espagne)

Thesis defended by Fei GAO

Tuesday, june 22, 2021. Study of the molecular mechanisms controlling iron homeostasis in plants

Thesis defended by Kevin Robe

January 28 2021 – Location, dynamics and role of coumarins in iron nutrition in Arabidopsis thaliana

Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process

A new publication from Kevin’s PhD thesis (Robe et al., 2021 – New Phytol, doi: 10.1111/nph.17090)

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, doi: 10.1074/jbc.RA119.011034). An article which was selected by the JBC editorial team to celebrates a few of the new insights, advances and tools that moved scientific research forward in 2020

The Coumarins: Secondary Metabolites Playing a Primary Role in Plant Nutrition and Health

Interested in coumarins or plant nutrition and health? Here is a recent review on the role of coumarins in plant nutrition and health prepared by Kevin (Robe et al., 2021 – Trends Plant Sci, doi: 10.1016/j.tplants.2020.10.008)

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, doi: 10.3389/fpls.2019.00712)

Identification of client iron-sulfur proteins of the chloroplastic NFU2 transfer protein in Arabidopsis thaliana

Some news in the biogenesis of iron-sulfur centers and the role of NFU2 in this process, a work led by Nathalie which follows the one of Brigitte (Berger et al., 2020 – J Exp Bot, doi: 10.1093/jxb/eraa166)

Transcriptional integration of the plant responses to iron availability

Interested by how regulatory networks control gene expression or by the regulation of iron homeostasis, here is a recent review to understand the complexity of the molecular mechanisms that plants have evolved to maintain the homeostasis of their nutrients. (Fei and Dubos, 2020 – J Exp Bot, doi: 10.1093/jxb/eraa556)

Iron–sulfur protein NFU2 is required for branched-chain amino acid synthesis in Arabidopsis roots

Some news on the iron–sulfur biogenesis, a manuscript issued from Brigitte’s work (Touraine et al., 2019 – J Exp Bot, doi: 10.1093/jxb/erz050)

Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3

A novel paper from Nicolas’s PhD thesis (Tissot et al., 2019 – New Phytol, doi: 10.1093/jxb/erz050)

The Transcription Factor bHLH121 Interacts with bHLH105 (ILR3) and its Closest Homologs to Regulate Iron Homeostasis in Arabidopsis

A new paper from Fei’s PhD thesis (Gao et al., 2020 – Plant Cell, doi: 10.1105/tpc.19.00541)