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1. Sulphur availability modulates Arabidopsis thaliana responses to iron deficiency

Author

Kevin Robe, Fei Gao, Pauline Bonillo, Nicolas Tissot, Frédéric Gaymard, Pierre Fourcroy, Esther Izquierdo, Christian Dubos, Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
Chlorophyll, Pigments, Leaves, Chloroplasts, Transcription, Genetic, Arabidopsis thaliana, Physiology, [SDV]Life Sciences [q-bio], Arabidopsis, Gene Expression, Plant Science, Gene Expression Regulation, Plant, Medicine and Health Sciences, Homeostasis, Materials, Plant Anatomy, Mineral nutrient, Nutritional Deficiencies, Eukaryota, Iron Deficiencies, Plants, Chemistry, Experimental Organism Systems, Micronutrient Deficiencies, Physical Sciences, Medicine, Cellular Structures and Organelles, Cellular Types, Research Article, Chemical Elements, Science, Plant Cell Biology, Iron, Materials Science, Brassica, Research and Analysis Methods, Fe homeostasis, Mn, Model Organisms, Plant and Algal Models, Plant Cells, Genetics, Zn, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Nutrition, Manganese, Organic Pigments, Organisms, Biology and Life Sciences, Cell Biology, Iron Deficiency, Animal Studies, Physiological Processes, Fe deficiency, Sulfur
Abstract

International audience; Among the mineral nutrients that are required for plant metabolism, iron (Fe) and sulphur (S) play a central role as both elements are needed for the activity of several proteins involved in essential cellular processes. A combination of physiological, biochemical and molecular approaches was employed to investigate how S availability influences plant response to Fe deficiency, using the model plant Arabidopsis thaliana. We first observed that chlorosis symptom induced by Fe deficiency was less pronounced when S availability was scarce. We thus found that S deficiency inhibited the Fe deficiency induced expression of several genes associated with the maintenance of Fe homeostasis. This includes structural genes involved in Fe uptake (i.e. IRT1, FRO2, PDR9, NRAMP1) and transport (i.e. FRD3, NAS4) as well as a subset of their upstream regulators, namely BTS, PYE and the four clade Ib bHLH. Last, we found that the over accumulation of manganese (Mn) in response to Fe shortage was reduced under combined Fe and S deficiencies. These data suggest that S deficiency inhibits the Fe deficiency dependent induction of the Fe uptake machinery. This in turn limits the transport into the root and the plant body of potentially toxic divalent cations such as Mn and Zn, thus limiting the deleterious effect of Fe deprivation

Published
2020

2. TCTP and CSN4 control cell cycle progression and development by regulating CULLIN1 neddylation in plants and animals

Author

Mohammed Bendahmane, Pierre Chambrier, Garance Pontier, Victor Girard, Barbara Wipperman, Cécile Raynaud, Nicolas Tissot, Véronique Boltz, Moussa Benhamed, Florian Brioudes, Bertrand Mollereau, Julie Savarin, Judit Szécsi, Léo Betsch, Reproduction et développement des plantes (RDP), École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), SFR Biosciences, École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de biologie et modélisation de la cellule (LBMC UMR 5239), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-École normale supérieure - Lyon (ENS Lyon)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), This work was supported by funds from the French 'Agence Nationale de la Recherche' grants ANR-09-BLAN-0006 and ANR-13-BSV7-0014, by the 'Biologie et Amélioration des Plantes' Department of the French 'Institut National de la Recherche Agronomique', by the 'Ecole Normale Supérieure de Lyon', by Rijk Zwaan company and by the CIFRE program of the ANRT., ANR-09-BLAN-0006,PetalSize,Etudes Moléculaires et Génétiques de la Morphogenèse du Pétale(2009), ANR-13-BSV7-0014,DODO,Identification et caractérisation des mutations DOMINANT DOUBLE (DODO) and DOUBLE FLOWER (DF) chez le pétunia et la rose(2013), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Bodescot, Myriam, Blanc - Etudes Moléculaires et Génétiques de la Morphogenèse du Pétale - - PetalSize2009 - ANR-09-BLAN-0006 - Blanc - VALID, Blanc 2013 - Identification et caractérisation des mutations DOMINANT DOUBLE (DODO) and DOUBLE FLOWER (DF) chez le pétunia et la rose - - DODO2013 - ANR-13-BSV7-0014 - Blanc 2013 - VALID, and Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11)

Subjects
Leaves, Embryology, Cancer Research, Arabidopsis, Plant Science, 0302 clinical medicine, Ubiquitin, Medicine and Health Sciences, Drosophila Proteins, Cell Cycle and Cell Division, Flowering Plants, Genetics (clinical), 0303 health sciences, biology, Drosophila Melanogaster, Plant Anatomy, eucaryote, Eukaryota, Animal Models, Plants, Cullin Proteins, 3. Good health, Cell biology, Insects, Experimental Organism Systems, Cell Processes, Drosophila, CUL1, prolifération, Anatomy, Microtubule-Associated Proteins, Cell Division, Cullin, Research Article, lcsh:QH426-470, Arthropoda, Arabidopsis Thaliana, Brassica, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, Research and Analysis Methods, 03 medical and health sciences, Model Organisms, Downregulation and upregulation, Plant and Algal Models, Ocular System, Tobacco, Translationally-controlled tumor protein, Genetics, Animals, Molecular Biology, [SDV.BC] Life Sciences [q-bio]/Cellular Biology, Ecology, Evolution, Behavior and Systematics, Cell Proliferation, Adaptor Proteins, Signal Transducing, 030304 developmental biology, Arabidopsis Proteins, COP9 Signalosome Complex, Cell growth, Embryos, Organisms, Biology and Life Sciences, Cell Biology, Cell Cycle Checkpoints, Invertebrates, cycle cellulaire, lcsh:Genetics, Animal Studies, biology.protein, Eyes, Neddylation, Head, 030217 neurology & neurosurgery, Developmental Biology
Abstract

Translationally Controlled Tumor Protein (TCTP) controls growth by regulating the G1/S transition during cell cycle progression. Our genetic interaction studies show that TCTP fulfills this role by interacting with CSN4, a subunit of the COP9 Signalosome complex, known to influence CULLIN-RING ubiquitin ligases activity by controlling CULLIN (CUL) neddylation status. In agreement with these data, downregulation of CSN4 in Arabidopsis and in tobacco cells leads to delayed G1/S transition comparable to that observed when TCTP is downregulated. Loss-of-function of AtTCTP leads to increased fraction of deneddylated CUL1, suggesting that AtTCTP interferes negatively with COP9 function. Similar defects in cell proliferation and CUL1 neddylation status were observed in Drosophila knockdown for dCSN4 or dTCTP, respectively, demonstrating a conserved mechanism between plants and animals. Together, our data show that CSN4 is the missing factor linking TCTP to the control of cell cycle progression and cell proliferation during organ development and open perspectives towards understanding TCTP’s role in organ development and disorders associated with TCTP miss-expression., Author summary During organism development, the correct implementation of organs with unique shape, size and function, is the result of coordinated cellular processes, such as cell proliferation and expansion. Deregulation of these processes affect human health and can lead to severe diseases. While plants and animals have largely diverged in several aspects, some biological functions, such as cell proliferation, are conserved between these kingdoms. Previously we reported that the Translationally Controlled Tumor Protein (TCTP), a highly-conserved protein among all eukaryotes, positively regulates cell proliferation and this role is conserved between plants and animals. In agreement with these data, animals TCTP was reported to highly accumulate in tumor cells, and thus represents a target for cancer research and therapies. To discover how TCTP regulates cell proliferation, we conducted studies to identify factors acting in the TCTP pathway. Using the model plant Arabidopsis, we identified that TCTP fulfil its role by interacting with CSN4, a subunit of the conserved COP9 complex. TCTP interferes with the role of COP9 to regulate the downstream complex CRL known to control cell proliferation in eukaryotes. We further demonstrate that this role is conserved in the fly Drosophila, thus corroborating the conservation of TCTP pathway between plants and animals. We believe that, the data here will provide exciting perspectives, beyond plant research, that will help understand developmental disorders associated with TCTP misfunction, such as cancer.

Published
2019

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

Author

Jean-François Briat, Fei Gao, Esther Izquierdo, Hannetz Roschzttardtz, Antoine Martin, Jossia Boucherez, Florence Vignols, Susana Grant-Grant, Frédéric Gaymard, Nicolas Tissot, Kevin Robe, Moussa Benhamed, Fanny Bellegarde, Romain Marcelin, Christian Dubos, Amel Maghiaoui, Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), China Agricultural University (CAU), Plateforme de Spectrométrie de Masse Protéomique - Mass Spectrometry Proteomics Platform (MSPP), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA), Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
0106 biological sciences, 0301 basic medicine, ferritins, Transcription, Genetic, Arabidopsis thaliana, Physiology, Arabidopsis, Repressor, bHLH105, Plant Science, Genes, Plant, 01 natural sciences, Models, Biological, Plant Roots, E-Box Elements, 03 medical and health sciences, iron, Gene Expression Regulation, Plant, Basic Helix-Loop-Helix Transcription Factors, PYE, Homeostasis, Promoter Regions, Genetic, Gene, ComputingMilieux_MISCELLANEOUS, biology, Basic helix-loop-helix, Chemistry, Arabidopsis Proteins, Structural gene, basic helixÀloopÀhelix, biology.organism_classification, Cell biology, Ferritin, Plant Leaves, [SDV.BV.AP]Life Sciences [q-bio]/Vegetal Biology/Plant breeding, 030104 developmental biology, Seedlings, basic helix-loop-helix, biology.protein, home- ostasis, ILR3, Function (biology), 010606 plant biology & botany, Protein Binding
Abstract

International audience; Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency and to excess is still to be determined. In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess. A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant's response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity. Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor.

Published
2019

4. Facilitated Fe Nutrition by Phenolic Compounds Excreted by the Arabidopsis ABCG37/PDR9 Transporter Requires the IRT1/FRO2 High-Affinity Root Fe(2+) Transport System

Author

Nicolas Tissot, Frédéric Gaymard, Christian Dubos, Pierre Fourcroy, Jean-François Briat, Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
0106 biological sciences, 0301 basic medicine, FMN Reductase, Iron, iron transport, Arabidopsis, chemistry.chemical_element, ATP Binding Cassette Transporter, Subfamily G, Plant Science, Biology, 01 natural sciences, Oxygen, Plant Roots, Ferrous, Metal, 03 medical and health sciences, Nutrient, Phenols, Botany, medicine, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Chelation, Cation Transport Proteins, Molecular Biology, ComputingMilieux_MISCELLANEOUS, Arabidopsis Proteins, Biological Transport, root, 030104 developmental biology, chemistry, visual_art, Environmental chemistry, Soil water, visual_art.visual_art_medium, Ferric, IRT1/FRO2, Plant nutrition, 010606 plant biology & botany, medicine.drug
Abstract

Iron (Fe) is an essential metal nutrient for plant productivity and plant product quality (Briat et al., 2015). Fe exists under two forms, ferrous (Fe2+) or ferric (Fe3+), and is very reactive with oxygen, explaining why Fe plant nutrition is dependent upon both Fe chelation and Fe reduction. Fe availability in the soil is pH dependent, this metal being particularly insoluble in its ferric form in calcareous soils, representing one-third of the world’s cultivated soils. Consequently, plants grown on these soils, in particular non-graminaceous plants, often suffer from Fe deficiency, which alters their growth.

Published
2016

5. Iron around the clock

Author

Nicolas Tissot, Baptiste Castel, Christian Dubos, Frédéric Gaymard, Guilhem Reyt, Jossia Boucherez, Céline Duc, Jean-François Briat, Jonathan Przybyla-Toscano, Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and Ministere de l'enseignement superieur et de la recherche

Subjects
Chloroplasts, Light, Arabidopsis thaliana, Iron, Photoperiod, Period (gene), Circadian clock, Retrograde signalling, Arabidopsis, Plant Science, Biology, Chloroplast, Circadian Clocks, Iron homeostasis, Genetics, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Epigenetics, Phytochrome, Mechanism (biology), Ecology, General Medicine, biology.organism_classification, Circadian Rhythm, Cell biology, Signalling, Retrograde signaling, Agronomy and Crop Science
Abstract

International audience; Carbon assimilation, a key determinant of plant biomass production, is under circadian regulation. Light and temperature are major inputs of the plant clock that control various daily rhythms. Such rhythms confer adaptive advantages to the organisms by adjusting their metabolism in anticipation of environmental fluctuations. The relationship between the circadian clock and nutrition extends far beyond the regulation of carbon assimilation as mineral nutrition, and specially iron homeostasis, is regulated through this mechanism. Conversely, iron status was identified as a new and important input regulating the central oscillator, raising the question of the nature of the Fe-dependent signal that modulates the period of the circadian clock. Several lines of evidence strongly suggest that fully developed and functional chloroplasts as well as early light signalling events, involving phytochromes, are essential to couple the clock to Fe responses. Nevertheless, the exact nature of the signal, which most probably involves unknown or not yet fully characterized elements of the chloroplast-to-nucleus retrograde signalling pathway, remains to be identified. Finally, this regulation may also involves epigenetic components.

Published
2014

6. 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

Author

Jean-François Briat, Nicolas Tissot, Frédéric Gaymard, Jossia Boucherez, Eric Lacombe, Stéphane Mari, Marc Bournier, Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Résistance des plantes aux bio-agresseurs (UMR RPB), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université Montpellier 2 - Sciences et Techniques (UM2), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université Montpellier 2 - Sciences et Techniques (UM2)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), and Gaymard, Frederic

Subjects
0106 biological sciences, Iron, [SDV]Life Sciences [q-bio], Response element, Mutant, Arabidopsis, homéostasie du fer, Plant Biology, Biology, Genes, Plant, 01 natural sciences, Biochemistry, Phosphates, fer, Redox, 03 medical and health sciences, Gene Expression Regulation, Plant, Homeostasis, Promoter Regions, Genetic, Molecular Biology, Transcription factor, levure, 030304 developmental biology, Regulation of gene expression, 0303 health sciences, Metal Homeostasis, Vegetal Biology, gène transporteur, Arabidopsis Proteins, fungi, food and beverages, Promoter, Cell Biology, Plant, Iron Metabolism, Ferritin, Regulatory sequence, Ferritins, biology.protein, Starvation response, Biologie végétale, 010606 plant biology & botany, Signal Transduction, Transcription Factors, Autre (Sciences du Vivant)
Abstract

International audience; A yeast one-hybrid screening allowed the selection of PHR1 as a factor that interacted with the AtFer1 ferritin gene promoter. In mobility shift assays, PHR1 and its close homologue PHL1 (PHR1-like 1) interact with Element 2 of the AtFer1 promoter, containing a P1BS (PHR1 binding site). In a loss of function mutant for genes encoding PHR1 and PHL1 (phr1 phl1 mutant), the response of AtFer1 to phosphate starvation was completely lost, showing that the two transcription factors regulate AtFer1 expression upon phosphate starvation. This regulation does not involve the IDRS (iron-dependent regulatory sequence) present in the AtFer1 promoter and involved in the iron-dependent regulation. The phosphate starvation response of AtFer1 is not linked to the iron status of plants and is specifically initiated by phosphate deficiency. Histochemical localization of iron, visualized by Perls DAB staining, was strongly altered in a phr1 phl1 mutant, revealing that both PHR1 and PHL1 are major factors involved in the regulation of iron homeostasis.

Published
2013

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