Cytosolic and nuclear calcium signalling in plants

Research Topics

Environmental constraints limit crops productivity and basic research is essential to provide a  sufficient  knowledge to enhance stress tolerance in plants of agronomic interest. In their environment, in order to face these multiple stresses, plants use calcium as a second messenger   to mediate appropriate adaptive responses. Our group aims at understanding the mechanisms involved in calcium-dependent signaling pathways that participate to immune responses in plants. Our studies focus on the specific role of calcium-dependent protein kinases (CDPKs) and calmodulin-like proteins (CMLs) that are two plant -specific families of calcium sensors.

Calcium Imaging

Contacts : Christian MAZARS

Very often, variation in calcium concentration is part of plant cell responses to stimuli. For a long time, the cytosol was thought to be the only active cellular compartment in regards to calcium signalling. It is now clear that other cellular compartments such as plastids, mitochondria or nuclei also participate in shaping a specific calcium response according to the applied stimulus (Xiong et al. 2006). This subcellular localization of the calcium signal combined with other parameters such as intensity, duration, shape or frequency define the so-called “calcium signature” (McAinsh & Pittman 2009).

By using the jellyfish-derived calcium probe AEQUORIN, we are able to follow real-time calcium variations in the cytosol and the nucleus. In presence of the chromophore coelentarazine, apo-aequorin is capable of binding 3 calcium ions. This provokes a conformational change followed by an intramolecular oxidation that emits blue light at 468nm. The light emission is proportional to the calcium concentration and can be captured by a sensitive PMT-based luminometer.

Using this approach, our group has demonstrated:

  • The contribution of nuclei in defining a specific calcium signature
  • The autonomy of nuclei in producing a calcium signal when challenged with external stimuli
  • The possibility for nuclei to control, independently or via the cytosol, responses implicating calcium signalling.

We now seek to develop new imaging approaches and “low-light” experimental setups allowing to monitor in real-time,  calcium variations at the plant scale or at the organ scale in responses to external stimuli, thereby harnessing  most of the high dynamic range of Aequorin.

We are also exploring the possibilities brought by another calcium probe, the BRET (Bioluminescence Resonance Energy Transfert) sensor G5A. G5A has a 3 to 5 times higher signal-to-noise ratio than aequorin (Xiong et al. 2014).

Collaborations:

Barker D. , De Carvalho-Niebel F. : http://www6.toulouse.inra.fr/lipm_e…

Le Ru A. : http://www.fraib.fr/Ressources-tech…

Mithöfer A. : http://www.ice.mpg.de/ext/bioorgani…

Xiong T.C. : https://www1.montpellier.inra.fr/wp-inra/bpmp/recherche/les-equipes/tsf/

Literature cited :

McAinsh MR, Pittman JK. (2009) Shaping the calcium signature. New Phytol. 181(2):275-94.

Alonso MT and Garcia-Sancho J. (2011) Nuclear Ca2+Signalling. Cell Calcium 49:280-289

Xiong TC, Ronzier E, Sanchez F, Corratgé-Faillie C, Mazars C, Thibaud JB.(2014). Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci.5:43.

Sphingolipid signalling, cell death, 14-3-3 proteins and calcium regulation

Contacts :   Valérie COTELLE,  Malick MBENGUE   Christian MAZARS

Studies of plant nuclear calcium signalling led us to consider sphingolipids as putative activators of nuclear-localized calcium channel, a role that sphingolipids fulfill in animals by activating nuclear TRP channels (Grimm et al., 2005). Sphingoid Long Chain Bases (LCBs), metabolic precursors of ceramides and other complex lipids, are now recognized as potent signalling molecules governing eukaryotic cell fate.

Our group and others have shown that LCBs can induce programmed cell death (PCD) in plants or plant cell cultures. We showed that among the large LCB family, only non-phosphorylated forms (sphingosine, dihydrosphingosine, dimethylsphingosine) can induce nuclear calcium variations in cells or purified nuclei displaying various characteristics depending on the compound or the condition tested (Xiong et al., 2008).

In addition, we showed that the two most abundant plant LCBs (phytosphingosine and dihydrosphingosine) can induce PCD of Arabidopsis or tobacco cells. We further aim at better understanding how calcium signalling intersects with this activity.

Further, the mycotoxin Fumonisin B1 (FB1) is a structural analogue of LCBs that can induce PCD when infiltrated in plants. We contributed in the description of the first molecular events associated with FB1 or LCBs applications:

  • Increase in cytosolic calcium concentration
  • Increase in free LCBs
  • A delayed nuclear calcium increase
  • Reactive oxygen species and nitric oxide bursts

A pharmacological approach demonstrated that nuclear calcium signalling is critical to mount the PCD process in response to LCB applications, whereas ROS and NO bursts are dispensable (Lachaud et al. 2010; Lachaud et al. 2011; Da Silva et al. 2011).

In Arabidopsis, the LCB-induced calcium variations activate a calcium-dependent protein kinase (CPK3) which is sequestered by a 14-3-3 dimer. Upon FB1 or LC application, CPK3 phosphorylates a critical residue involved in 14-3-3 dimerization, allowing CPK3 release and cleavage. Reverse genetics determined that CPK3 is a positive regulator of the PCD response triggered by FB1 (Lachaud et al. 2013). The NO burst observed in tobacco cell culture after LCB treatment seems to participate in the accumulation of the glyceraldehyde-3-phosphate deshydrogenase (GAPDH) in the nucleus, where the enzyme is found nitrosylated.

Focusing on the plant model Arabidopsis, our next objectives are to :

  1. Understand how calcium and its compartmentalization controls the LCBs signalling pathway leading to PCD, via protein-protein interactions (CPK3/14-3-3) and phosphorylation events.?
  2. Further characterize the regulation processes and roles of 14-3-3s and their targets in LCBs-induced PCD.
  3. Decipher FB1 mode(s) of action leading to plant cell death

Collaborations

Le Ru A. : http://www.fraib.fr/fraib_eng/Techn…

Xiong T.C. : https://www1.montpellier.inra.fr/wp-inra/bpmp/recherche/les-equipes/tsf/Boudsocq M. :  http://www.ips2.u-psud.fr/spip.php?article40

Van der Hoorn R. : http://www.plantchemetics.org/index…

Literature cited and articles from the group related to the topic

Grimm C, Kraft R, Schultz G, Harteneck C. (2005). Activation of the melastatin-related cation channel TRPM3 by D-erythro-sphingosine [corrected]. Mol Pharmacol. 67(3):798-805

Calcium sensors and environmental stresses

Contacts :   Didier ALDON,   Jean-Philippe GALAUD,   Benoît RANTY,   Christian MAZARS

Like all living organisms, plants have to face environmental constraints that can be of biotic nature such as pathogens (e.g. bacteria, fungi, oomycetes, viruses, insects) and of abiotic nature such as drought, soil salinity, air pollution, extreme temperatures and mechanical injuries. To adapt to adverse growth conditions, plants must be able to perceive the nature and the strength of stimuli, interpret them and activate appropriate physiological responses. Among signalling elements that are involved in plant stress responses, Ca2+ ions are among the earliest actors that coordinate plant adaptive responses. The complex spatiotemporal patterns of Ca2+ influx at cellular and tissue levels (frequency, amplitude, and distribution within the cell) likely carry information and are defined as “Ca2+ signature”. This Ca2+message further needs to be decoded and relayed by Ca2+-binding proteins termed Ca2+ sensors in order to carry out the appropriate cell response. The molecular bases of the underlying calcium signalling pathways are largely unknown.

Plants can perceive a plethora of environmental signals that lead to calcium variations within the cells. These variations are important in mounting the appropriate response.

Among the proteins capable of decoding calcium signals, calmodulin (CaM) is found in all eukaryotes and can modulate the activity of several targets. In addition, plants possess a specific repertoire of CaM-related proteins termed CML for calmodulin-like. For the vast majority of these CMLs, no physiological role is clearly established (Perochon et al. 2011, Zhu et al. 2015).

Using Arabidopsis and tomato as model plants, our group works on extending our knowledge on selected CaM and CMLs, as well as their targets during stresses tolerance responses (Ghorbel et al. 2015). For example, we showed that CML8 and CML9 act as regulators of abiotic and/or biotic stress responses (Magnan et al. 2008 ; Leba et al, 2012 ; Zhu et al. 2017).

Our objectives are to extend our initial work on CMLs and on their targets that we identified. A particular interest is given to the contribution of these proteins in plant stress responses including changes in temperature and pathogen responses.

 

Collaborations:

Projet ANR CaPPTure* (2018-2021) in collaboration with:

*Project labelled by the GIS BV and the Pôle de Competitivité AGRI SUD-OUEST INNOVATION

Berthomé R., Toulouse, France : http://www6.toulouse.inra.fr/lipm/R…

Claire Lurin, Saclay, France : http://www.ips2.u-psud.fr

Abdel Bendhamane, Saclay, France : http://www.ips2.u-psud.fr

Others:

Xiaoyang Zhu, Guangzhou, South China Agricultural University, China

Snedden W, Kingston, Canada. : https://sneddenlab.wordpress.com/research/

Mithöfer A., Iena, Allemagne : http://www.ice.mpg.de/ext/bioorgani…

Hanin M. Sfax, Tunisie : http://www.cbs.rnrt.tn/

Member of the « Plant Resistance network » set up by JB Morel and L Deslandes (INRA)

Member of the Groupement d’Intérêt Scientifique « Biotechnologies Vertes » (GIS BV)

Local collaborations:

Projet FRAIB- Labex Tulip avec F. Roux « Effet de changements climatiques sur le tradeoff croissance/réponse aux bioagresseurs chez Arabidopsis thaliana ».

Publications

2018

Aldon D, Mbengue M, Mazars C, Galaud JP (2018) Calcium Signalling in Plant Biotic Interactions. Int J Mol Sci. [http://www.mdpi.com/1422-0067/19/3/665]

2017

Zhu X, Perez M, Didier Aldon D & JP Galaud (2017) Respective contribution of CML8 and CML9, two arabidopsis calmodulin-like proteins, to plant stress responses.[http://www.tandfonline.com/doi/full…]

Ghorbel M., Cotelle V., Ebel C., Zaidi I., Ormancey M., Galaud J.P., Hanin M. (2017) Regulation of the wheat MAP kinase phosphatase 1 by 14-3-3 proteins. [http://www.sciencedirect.com/scienc…] 257, 37–47.

Zhu X, Robe E, Jomat L, Aldon A, Mazars C, Galaud JP (2017) Calmodulin-like 8 contributes to plant immunity.[https://academic.oup.com/pcp/articl…] 58(2):307-319

Ormancey M, Thuleau P, Mazars C, Cotelle V (2017) CDPKs and 14-3-3 Proteins : Emerging Duo in Signaling. Trends Plant Sci. S1360-1385(16)30190-X.

2016

Testard A, Da Silva D, Ormancey M, Pichereaux C, Pouzet C, Jauneau A, Grat S, Robe E, Brière C, Cotelle V, Mazars C, Thuleau P (2016) Calcium- and Nitric Oxide-Dependent Nuclear Accumulation of Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenase in Response to Long Chain Bases in Tobacco BY-2 Cells. Plant Cell Physiol 57 (10) :2221-2231

Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C (2016) Calcium sensors as key hubs in plant responses to biotic and abiotic stresses Front. Plant Sci 7:327

Cotelle V, Leonhardt N (2016) 14-3-3 proteins in guard cell signaling. Front.Plant Sci 6:12

Mazars C ; Ranty B ; Aldon D ; Oelmüller R ; Galaud J-P ; Mithöfer A (2016) CMLs control host-plant interactions.Endocytobiosis and Cell Research 27:13-19

2015

Ghorbel M, Zaidi I, Robe E, Ranty B, Mazars C, Galaud JP, Hanin M (2015) The activity of the wheat MAP kinase phosphatase 1 is regulated by manganese and by calmodulin. Biochimie 108 : 13-19

Zhu X, Dunand C, Snedden W, Galaud JP (2015) CaM and CML emergence in the green lineage. Trends Plant Sci. doi:10.1016/j.tplants.2015.05.010

2014

Coursol S, Fromentin J, Noirot E, Brière C, Robert F, Morel J, Liang Y-K, Lherminier J, Simon-Plas F (2014) Long-chain bases and their phosphorylated derivatives differentially regulate cryptogein-induced production of reactive oxygen species in tobacco BY-2 cells. New Phytologist 205(3), 1239-49.

Kittang A, Iversen T, Fossum K, Mazars C, CarneroDiaz E, Boucheron−Dubuisson E, Le Disquet I, Herranz R, Pereda−Loth V, Medina FJ (2014) Exploration of plant growth and development using the European Modular Cultivation System facility on the International Space Station. Plant Biology 16(3), 528-538.

Mazars C, Brière C, Grat S, Pichereaux C, Rossignol M, Pereda-Loth V, Eche B, Boucheron-Dubuisson E, Le Disquet I, Medina FJ, Graziana A, Carnero-Diaz E (2014) Microgravity induces changes in microsome-associated proteins of Arabidopsis seedlings grown on board the international space station. PLoS One 9(3) : e91814. doi:10.1371/journal.pone.0091814

Mazars C, Brière C, Grat S, Pichereaux C, Rossignol M, Pereda-Loth V, Eche B, Boucheron-Dubuisson E, Le Disquet I, Medina FJ, Graziana A, Carnero-Diaz E (2014) Microsome-associated proteome modifications of Arabidopsis seedlings grown on board the International Space Station reveal the possible effect on plants of space stresses other than microgravity. Plant Signal. Behav. 9. e29637

Ronzier E, Sanchez C-F, Prado K, Briere C, Leonhard N, Thibaud J-B, Xiong T-C (2014). CPK13, a non-canonical CPK, specifically inhibits KAT2 and KAT1 Shaker channels and reduces stomatal opening. Plant Physiol. doi:10.1104/pp.114.240226

Xiong TC, Ronzier E, Sanchez F, Corratgé-Faillie C, Mazars C, Thibaud JB (2014) Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci 5:43. doi:10.3389/fpls.2014.00043

2013

Cheval C, Aldon D, Galaud JP, Ranty B (2013) Calcium/calmodulin-mediated regulation of plant immunity. Biochimica et Biophysica Acta 1833, 1766-1771.

Lachaud C, Prigent E, Thuleau P, Grat S, Da Silva D, Brière C, Mazars C, Cotelle V (2013) 14-3-3-regulated Ca2+-dependent protein kinase CPK3 is required for sphingolipid-induced cell death in Arabidopsis Cell Death and Differentiation 20(2), 209-217.

Pujol B, Galaud JP (2013) A practical guide to quantifying the effect of genes underlying adaptation in a mixed genomics and evolutionary ecology approach. Acta Botanica Gallica 160, 197-204.

Thuleau P, Aldon D, Cotelle V, Briere C, Ranty B, Galaud JP, Mazars C (2013) Relationships between calcium and sphingolipid-dependent signalling pathways during the early steps of plant-pathogen interactions. Biochimica et Biophysica Acta 1833, 1590-1594.

2012

Leba LJ, Perochon A, Cheval C, Ranty B, Galaud JP, Aldon D (2012) CML9, a multifunctional Arabidopsis thaliana calmodulin-like protein involved in stress responses and plant growth ? Plant Signal Behav. 7(9). PMID : 22899061.

Leba LJ, Cheval C, Ortiz-Martín I, Ranty B, Beuzón CR, Galaud JP, Aldon D (2012) CML9, an Arabidopsis calmodulin-like protein, contributes to plant innate immunity through a flagellin-dependent signalling pathway. Plant J. 71(6):976-89. PubMed PMID : 22563930.

Ranty B, Cotelle V, Galaud JP., Mazars C (2012) Nuclear calcium signaling and its involvement in transcriptional regulation in plants. Adv Exp Med Biol 740:1123-43. Invited review

Thuleau P, Briere C, Mazars C (2012) Recent advances in plant cell nuclear signalling. Mol Plant. 5(5):968-70. Invited Highlight.

2011

Amelot N, Dorlhac de Borne F, San Clemente H, Grima-Pettenati J, Mazars C, Brière C (2011) Transcriptome analysis of tobacco BY-2 cells elicited by cryptogein reveals new potential actors of calcium-dependent and calcium-independent plant defense pathways. Cell Calcium. 51(2):117-30

Amelot N, Carrouche A, Danoun S, Bourque S, Haiech J, Pugin A, Ranjeva R, Grima-Pettenati J, Mazars C, Briere C (2011) Cryptogein, a fungal elicitor, remodels the phenylpropanoid metabolism of tobacco cell suspension cultures in a calcium-dependent manner. Plant Cell Env 34 : 149-161 texte

Aubert Y, Leba LJ, Cheval C, Ranty B, Vavasseur A, Aldon D, Galaud JP (2011) Involvement of RD20, a member of caleaosin family, in ABA-mediated regulation of germination in Arabidopsis thaliana. Plant Signal & Behav. 6 : 538-540

Canonne J, Marino D, Jauneau A, Pouzet C, Brière C, Roby D, Rivas S (2011) The Xanthomonas Type III Effector XopD Targets the Arabidopsis Transcription Factor MYB30 to Suppress Plant Defense. Plant Cell 23 : 3498-3511

Da Silva D, Lachaud C, Cotelle V, Briere C, Grat S, Mazars C, Thuleau P (2011) Nitric oxide production is not required for dihydrosphingosine-induced cell death in tobacco BY-2 cells. Plant Signal & Behav. 6(5) : 736-739

Lachaud C, Da Silva D, Amelot N, Beziat C, Briere C, Cotelle V, Graziana A, Grat S, Mazars C, Thuleau P (2011) Dihydrosphingosine-induced programmed cell death in tobacco BY-2 Cells is independent of H2O2 production. Mol Plant 4(2) : 310-318

Masclaux F, Galaud JP (2011) Heat-inducible RNAi for gene functional analysis in plants. In Methods in Molecular Biology “RNAi and Plant Gene Function Analysis. Methods and Protocols”, Vol. 744. Humana Press, pp37-55

Mazars C, Brière C, Bourque S, Thuleau P (2011) Nuclear calcium signaling : an emerging topic in plants. Biochimie 93(12) : 2068-2074

Mazars C, Thuleau P, Cotelle V, Brière C (2011) Calcium signaling and homeostasis in nuclei. In S Luan, ed, Coding and decoding of calcium signals in plants, Springer, pp7-24

Perochon A, Aldon D, Galaud JP, Ranty B (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93(12) : 2048-2053

Ranty B, Cotelle V, Galaud JP, Mazars C (2011) Nuclear calcium signaling and its involvement in transcriptional regulation in plants. In S Islam, ed, Calcium signaling Series : Advances In Experimental Medecine and Biology, vol. 740 ch. 50, Springer

2010

Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP (2010) RD20, a Stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51 : 1975-1987

Borges JP, Culerrier R, Aldon D, Barre A, Benoist H, Saurel O, Milon A, Didier A, Rouge P (2010) GATEWAY technology and E. coli recombinant system produce a properly folded and functional recombinant allergen of the lipid transfer protein of apple (Mal d 3). Protein Expr Purif 70 : 277-282

Dahan J, Wendehenne D, Ranjeva R, Pugin A, Bourque S (2010) Nuclear protein kinases : still enigmatic components in plant cell signalling. New Phytol 185 : 355-368

Froidure S, Canonne J, Daniel X, Jauneau A, Briere C, Roby D, Rivas S (2010) AtsPLA2-alpha nuclear relocalization by the Arabidopsis transcription factor AtMYB30 leads to repression of the plant defense response. Proc Natl Acad Sci U S A 107 : 15281-15286

Lachaud C, Da Silva D, Cotelle V, Thuleau P, Xiong TC, Jauneau A, Briere C, Graziana A, Bellec Y, Faure JD, Ranjeva R, Mazars C (2010) Nuclear calcium controls the apoptotic-like cell death induced by d-erythro-sphinganine in tobacco cells. Cell Calcium 47 : 92-100

Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3 : 706-718

Perochon A, Dieterle S, Pouzet C, Aldon D, Galaud JP, Ranty B (2010) Interaction of a plant pseudo-response regulator with a calmodulin-like protein. Biochem Biophys Res Commun. 398(4) : 747-751

Tasset C, Bernoux M, Jauneau A, Pouzet C, Brière C, Kieffer-Jacquinod S, Rivas S, Marco Y, Deslandes L (2010) Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathog 6 : e1001202

2009

Dagher R, Briere C, Feve M, Zeniou M, Pigault C, Mazars C, Chneiweiss H, Ranjeva R, Kilhoffer MC, Haiech J (2009) Calcium fingerprints induced by calmodulin interactors in eukaryotic cells. Biochim Biophys Acta 1793 : 1068-1077

Mazars C, Bourque S, Mithofer A, Pugin A, Ranjeva R (2009) Calcium homeostasis in plant cell nuclei. New Phytol 181 : 261-274

Mithofer A, Mazars C, Maffei ME (2009) Probing Spatio-temporal Intracellular Calcium Variations in Plants. Meth Mol Biol 479 : 79-92

Poutrain P, Mazars C, Thiersault M, Rideau M, Pichon O (2009) Two distinct intracellular Ca2+-release components act in opposite ways in the regulation of the auxin-dependent MIA biosynthesis in Catharanthus roseus cells. J Exp Bot 60 : 1387-1398

Vadassery J, Ranf S, Drzewiecki C, Mithofer A, Mazars C, Scheel D, Lee J, Oelmuller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59 : 193-206

2008

Bernoux M, Timmers T, Jauneau A, Briere C, de Wit PJ, Marco Y, Deslandes L (2008) RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20 : 2252-2264

Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56 : 575-589

Xiong TC, Coursol S, Grat S, Ranjeva R, Mazars C (2008) Sphingolipid metabolites selectively elicit increases in nuclear calcium concentration in cell suspension cultures and in isolated nuclei of tobacco. Cell Calcium 43 : 29-37

2007

Parre E, Ghars MA, Leprince AS, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savoure A (2007) Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiol 144 : 503-512

Ranty B, Aldon D, Galaud JP (2007) Regulation of gene expression by calmodulin in plants. Med Sci (Paris) 23 : 13-14

Walter A, Mazars C, Maitrejean M, Hopke J, Ranjeva R, Boland W, Mithofer A (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angew Chem Int Ed Engl 46 : 4783-4785

2006

Briere C, Xiong TC, Mazars C, Ranjeva R (2006) Autonomous regulation of free Ca2+ concentrations in isolated plant cell nuclei : a mathematical analysis. Cell Calcium 39 : 293-303

Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29 : 1956-1969

Gaulin E, Drame N, Lafitte C, Torto-Alalibo T, Martinez Y, Ameline-Torregrosa C, Khatib M, Mazarguil H, Villalba-Mateos F, Kamoun S, Mazars C, Dumas B, Bottin A, Esquerre-Tugaye MT, Rickauer M (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18 : 1766-1777

Hogg BV, Cullimore JV, Ranjeva R, Bono JJ (2006) The DMI1 and DMI2 early symbiotic genes of medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol 140 : 365-373

Lannoo N, Peumans WJ, Pamel EV, Alvarez R, Xiong TC, Hause G, Mazars C, Van Damme EJ (2006) Localization and in vitro binding studies suggest that the cytoplasmic/nuclear tobacco lectin can interact in situ with high-mannose and complex N-glycans. FEBS Lett 580 : 6329-6337

Laugesen S, Messinese E, Hem S, Pichereaux C, Grat S, Ranjeva R, Rossignol M, Bono JJ (2006) Phosphoproteins analysis in plants : a proteomic approach. Phytochem 67 : 2208-2214

Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171 : 249-269

Moreau M, Ranjeva R (2006) The calcium, an object of study, astonishing, no ? Med Sci (Paris) 22 : 1019

Ranty B, Aldon D, Galaud JP (2006) Plant Calmodulins and Calmodulin-Related Proteins : Multifaceted Relays to Decode Calcium Signals. Plant Signaling & Behavior 1 : 96-104

Xiong TC, Bourque S, Lecourieux D, Amelot N, Grat S, Briere C, Mazars C, Pugin A, Ranjeva R (2006) Calcium signaling in plant cell organelles delimited by a double membrane. Biochim Biophys Acta 1763 : 1209-1215

Xiong TC, Bourque S, Mazars C, Pugin A, Ranjeva R (2006) Cytosolic and nuclear calcium signalling in plants reply to biotic and abiotic stimuli. Med Sci (Paris) 22 : 1025-1028

2005

Leclercq J, Ranty B, Sanchez-Ballesta MT, Li Z, Jones B, Jauneau A, Pech JC, Latche A, Ranjeva R, Bouzayen M (2005) Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J Exp Bot 56 : 25-35

Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38 : 527-538

Masclaux FG, Galaud JP, Pont-Lezica R (2005) The riddle of the plant vacuolar sorting receptors. Protoplasma 226 : 103-108

Masclaux FG, Pont-Lezica R, Galaud JP (2005) Relationship between allelic state of T-DNA and DNA methylation of chromosomal integration region in transformed Arabidopsis thaliana plants. Plant Mol Biol 58 : 295-303

Olah B, Briere C, Becard G, Denarie J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44 : 195-207

2004

Charpenteau M, Jaworski K, Ramirez BC, Tretyn A, Ranjeva R, Ranty B (2004) A receptor-like kinase from Arabidopsis thaliana is a calmodulin-binding protein. Biochem J 379 : 841-848

Gressent F, Cullimore JV, Ranjeva R, Bono JJ (2004) Radiolabeling of lipo-chitooligosaccharides using the NodH sulfotransferase : a two-step enzymatic procedure. BMC Biochem 5 : 4

Masclaux F, Charpenteau M, Takahashi T, Pont-Lezica R, Galaud JP (2004) Gene silencing using a heat-inducible RNAi system in Arabidopsis. Biochem Biophys Res Commun 321 : 364-369

Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud JP, Ranjeva R, Ranty B (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38 : 410-420

Xiong TC, Jauneau A, Ranjeva R, Mazars C (2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. Plant J 40 : 12-21

2003

Centis-Aubay S, Gasset G, Mazars C, Ranjeva R, Graziana A (2003) Changes in gravitational forces induce modifications of gene expression in A. thaliana seedlings. Planta 218 : 179-185

Laval V, Masclaux F, Serin A, Carriere M, Roldan C, Devic M, Pont-Lezica RF, Galaud JP (2003) Seed germination is blocked in Arabidopsis putative vacuolar sorting receptor (atbp80) antisense transformants. J Exp Bot 54 : 213-221

Thuleau P, Leclerc C, Xiong TC, Mazars C, Leclerc C, Moreau M (2003) Luminous plant and animals or the expression of aequorin and “chameleon” probes : a new light in calcium signaling. J Soc Biol 197 : 291-300

Thesis

PhD students

Ambroise Testard (2014-2017) Rôle de la glycéraldéhyde 3-phosphate déshydrogénase nucléaire lors de mise en place de la mort cellulaire induite par les sphingolipides chez les végétaux.

Manon Perez(2014-2017) Analyse de la contribution de PRR2, un facteur de transcription de type GARP, dans la physiologie des plantes.

Mélanie Ormancey (2016) Signalisation calcique et protéines 14-3-3s dans la mort cellulaire induite par les sphingolipides chez les végétaux.

Xiaoyang Zhu (2016) Contribution de CML8 et CML11, deux “Calmodulin-like proteins” d’Arabidopsis thaliana dans les réponses aux stress.

Mouna Ghorbel (2015) Signalisation calcique et tolérance du blé aux stress abiotiques : rôles des calmodulines dans la modulation d’une MAPK Phosphatase (TMKP1). Thèse en co-tutelle (JP Galaud et M Hanin, Sfax, Tunisie)

Cécilia Cheval (2013) Contribution d’une “Calmodulin-like protein” CML9, et de son partenaire, le facteur de transcription de type GARP PRR2, à la mise en place des réactions de défense chez Arabidopsis thaliana.

Elsa Prigent (2013) Les protéines 14-3-3 et leurs cibles dans la voie de signalisation conduisant à la mort cellulaire programmée en réponse aux sphingolipides : régulation par le calcium.

Louis-Jérôme Leba (2011) Contribution d’AtCML9 aux réactions de défense mises en place en réponse à des stress biotiques chez Arabidopsis thaliana.

Daniel Da Silva (2011) Rôle du compartiment nucléaire dans la signalisation conduisant à la mort cellulaire en réponse aux sphingolipides chez des cellules de tabac BY2.

Yann Aubert (2011) Analyse fonctionnelle de deux protéines de liaison au calcium (AtCML9 et RD20) dans les réponses aux contraintes hydriques chez Arabidopsis thaliana.

Nicolas Amelot (2010) Couplage entre signalisation calcique et modulation du transcriptome en réponse à la cryptogéine chez le tabac. (en co-direction avec l’équipe “Régulation transcriptionnelle”).

Christophe Lachaud (2010) Mort cellulaire induite par les sphingolipides et signalisation calcique chez les végétaux.

Alexandre Perochon (2010) Signalisation calcium chez les plantes : Identification et caractérisation de partenaires de CML9, une protéine réceptrice des signaux calciques, impliquée dans les réponses aux stress de l’environnement chez Arabidopsis thaliana.

Fabienne Magnan (2007) Analyse fonctionnelle d’une protéine de type calmoduline d’Arabidopsis thaliana (AtCML9). Rôle dans les réponses des plantes aux contraintes de l’environnement.

Tou-Cheu Xiong (2005) Le noyau de la cellule végétale est-il autonome en matière de signalisation calcique ?

Elian Perruc (2004) Signalisation calcium chez les végétaux : Caractérisation d’une protéine affine à la calmoduline impliquée dans les réponses aux contraintes de l’environnement.

Frédéric Masclaux (2004) Analyse fonctionnelle d’une famille de protéines membranaires (AtBP-80) chez Arabidopsis thaliana : Recherche, obtention et caractérisation de mutants.

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