Calcium Signaling and Plant Immunity

Research Topics

In plants, one of the earliest common response that follows stimuli perception is a modulation of free calcium concentration within the cell. These calcium elevations can bear many shapes and are integral parts of the cell signaling that leads to specific plant responses. Our group aims at understanding how calcium through its spatio-temporal variations controls plant response specificity to biotic stresses. For this purpose, the group focus on the calcium signal itself but also on its decoders and more precisely on the large family of calmodulin-like proteins. Our models concern the pathogenic interaction between Arabidopsis and Tomato and bacteria belonging to the genus Pseudomonas and Ralstonia. Since 2016, the liverwort Marchantia polymorpha is also used in the group as a new plant model to study protein complexes associated with the generation of the calcium signal in response to biotic stress.

                Our scientific objectives are:

1) To identify calcium signal generating complexes by using immune Receptor-like Kinase signaling pathways as framework. This emerging scientific thematic is managed by M. Mbengue.

2) To decipher the contribution of plant specific calcium sensors (Calmodulin–like proteins and their targets) in immunity responses. This project is supported by the ANR CaPPTure project (2018-2022).

Calcium Imaging

Contacts : Sabine Grat-Simeone, Malick Mbengue, Didier Aldon, Jean-Philippe Galaud

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).


Barker D. , De Carvalho-Niebel F. :…

Le Ru A. :…

Mithöfer A. :…

Xiong T.C. :

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.

Identification of calcium signal generating complexes by using immune Receptor-like Kinase signaling pathways as a framework

Contacts :   Malick MBENGUE  Jean-Philippe Galaud

Pathogens recognition via plant surface immune receptors – receptors-like kinases (RLKs) – triggers a calcium influx across the plasma membrane into the cytosol that is required for downstream immune responses. Despite its critical importance for cell signaling, we only begin to discover the molecular actors that generate this calcium increase. Here, we hypothesize that the “calcium-machinery” is part of an immune-receptor protein complex as shown for some receptor-activated calcium channels in animal cells. That is why first, we propose to determine the architecture of a pre and post-activation plant-RLK signaling complex before describing the role of selected components in shaping the calcium signature. This is an emerging research axis in our group that aims at better understanding signaling events leading to the activation of defense responses, while providing important mechanistic insights into the generation of the calcium signal.

To date, Arabidopsis has been the model of choice for such studies but it becomes increasingly evident it suffers from functional redundancy that can hinder fast-paced reverse genetics studies. To alleviate this bottleneck, we propose to benefit from the liverwort Marchantia polymorpha, a tractable model recently introduced in our laboratory. Marchantia’s genome shows a reduction in the number of genes related to immune signaling, supporting the view that this species presents reduced functional redundancy. Our working RLK-model will be chitin perception by MpCERK1, the homologue of AtCERK1, a Lysin-Motif RLK (LysM-RLK) required for chitin perception in Arabidopsis and proximity labelling before performing reverse genetic studies in this species on selected candidates. 

Calcium sensors and environmental stresses

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

How these calcium variations are decoded and relayed to downstream effectors constitutes our second scientific objective. The decoding is carried out by relay proteins, such as calmodulin (CaM) that regulate the activity of target proteins following Ca2+-binding. Using molecular and genetic approaches, our group has revealed the physiological relevance of plant specific CaM related proteins, designated CML (Calmodulin-Like) in plant stress responses.

Since several years, we mainly focused on the importance of calcium signaling in response to biotic stimuli. Recently, thanks to the ANR CaPPTure project, we extend our work to other CMLs in Arabidopsis and in Tomato to evaluate their contribution in plant development and physiology in relation to simultaneous exposures to biotic and abiotic constraints. This work is part of a more general goal that is to better understand plant defence responses to pathogens according to changes of environmental conditions such as slight temperature variations. Indeed, a small increase in temperature (3 to 5 °C) significantly affects the resistance of plants to bacteria, fungi, viruses and insects, but only few data are available to explain this phenomenon. Although works have identified regulators of these stresses applied separately, our knowledge of the mechanisms allowing plants to simultaneously respond to multiple biotic and abiotic attacks remain fragmented. Since CMLs and their targets are at the crossroads of biotic and abiotic signaling pathways, our objectives are to decipher and understand their contribution in the responses of Arabidopsis and tomato to phytopathogenic bacteria (R. solanacearum and P. syringae). We evaluate the impact of the temperature on calcium signaling-induced-responses to these pathogens. This work will benefit of ongoing collaborations with R. Berthomé (LIPM, Toulouse), C. Lurin and A. Bendahmane, (IPS2, Paris) for plant-bacteria interaction studies, for identification of CML targets (Arabidopsis-Yeast two-hybrid platform) and for identification and generation of Tomato mutants by Tilling and CrispR-Cas9 technologies. This project also meets the objectives of the Labex “TULIP” by revealing the importance of calcium signaling and the effects of the environment on plant-microorganism interactions.

Overall, our team project aims to better characterize the regulatory networks associated to plant calcium signaling pathways activated by plant-microorganisms interactions. The project will be developed using different plant models to address both (i) the fundamental questions raised and (ii) to transfer acquired results to plants of agronomic interest.



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 :…

Claire Lurin, Saclay, France :

Abdel Bendhamane, Saclay, France :


Xiaoyang Zhu, Guangzhou, South China Agricultural University, China

Snedden W, Kingston, Canada. :

Mithöfer A., Iena, Allemagne :…

Hanin M. Sfax, Tunisie :

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)

Impact of ENvironment on plant immunity and pathogen VIrulencE (ENVIE) Network

Local collaborations:

S. Genin Team
L. Noel Team
L. Deslandes Team


Althiab-Almasaud R, Chen Y, Maza E, Djari A, Frasse P, Mollet JC, Mazars C, Jamet E, Chervin C., Plant J. 2021 Ethylene signaling modulates tomato pollen tube growth through modifications of cell wall remodeling and calcium gradient. Aug;107(3):893-908. doi: 10.1111/tpj.15353. Epub 2021 Jun 20.

Zhu X, Mazard J, Robe E, Pignoly S, Aguilar M, San Clemente H, Lauber E, Berthomé R, Galaud JP., 2021 The Same against Many: AtCML8, a Ca2+ Sensor Acting as a Positive Regulator of Defense Responses against Several Plant Pathogens. Int J Mol Sci. 2021 Sep 28;22(19):10469. doi: 10.3390/ijms221910469.

Xiong T, Tan Q, Li S, Mazars C, Galaud JP, Zhu X., 2021. Interactions between calcium and ABA signaling pathways in the regulation of fruit ripening.  J Plant Physiol. 2021 doi: 10.1016/j.jplph.2020.153309.

Ronzier E, Corratgé-Faillie C, Sanchez F, Brière C, Xiong TC.Ca2+-Dependent Protein Kinase 6 Enhances KAT2 Shaker Channel Activity in Arabidopsis thaliana. Int J Mol Sci. 2021 Feb 5;22(4):1596. doi: 10.3390/ijms22041596.


Barbacci A, Navaud O, Mbengue M, Barascud M, Godiard L, Khafif M, Lacaze A, Raffaele S. (2020) Rapid identification of an Arabidopsis NLR gene as a candidate conferring susceptibility to Sclerotinia sclerotiorum using time-resolved automated phenotyping. Plant J. 2020 Jul;103(2):903-917. doi: 10.1111/tpj.14747.

Sucher J, Mbengue M, Dresen A, Barascud M, Didelon M, Barbacci A, Raffaele S. (2020) Phylotranscriptomics of the Pentapetalae Reveals Frequent Regulatory Variation in Plant Local Responses to the Fungal Pathogen Sclerotinia sclerotiorum. Plant Cell. 2020 Jun;32(6):1820-1844. doi: 10.1105/tpc.19.00806.

Derbyshire M, Mbengue M, Barascud M, Navaud O, Raffaele S. (2020) Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance. Mol Plant Pathol. 2019 Sep;20(9):1279-1297. doi: 10.1111/mpp.12841.


Dell’Aglio E, Giustini C, Kraut A, Couté Y, Costa A, Decros G, Gibon Y, Mazars C, Matringe M, Finazzi G, Curien G. (2019) Identification of the Arabidopsis Calmodulin-Dependent NAD+ Kinase That Sustains the Elicitor-Induced Oxidative Burst. Plant Physiol. 181(4):1449-1458.

Bourque S, Lindermayr C, Mazars C., (2019) Post-translational Modifications in Plant Nuclear Signaling: Novel Insights Into Responses to Environmental Changes.  Front Plant Sci. 2019 Feb 11;10:104. doi: 10.3389/fpls.2019.00104

Peyraud R, Mbengue M, Barbacci A, Raffaele S (2019) Intercellular cooperation in a fungal plant pathogenfacilitates host colonization. Proc Natl Acad Sci USA 116 (8) 3193-3201


Aldon D, Mbengue M, Mazars C, Galaud JP (2018) Calcium Signalling in Plant Biotic Interactions. Int J Mol Sci. []

Favre L., Ortalo-Magné A., Pichereaux C., Gargaros A., Burlet-Schiltz O., Cotelle V. and Culioli G. (2018). Metabolome and proteome changes between biofilm and planktonic phenotypes of the marine bacterium Pseudoalteromonas lipolytica TC8. Biofouling. 34 : 132-148.

Heyer M, Scholz SS, Voigt D, Reichelt M, Aldon D, Oelmüller R, Boland W, Mithöfer A., 2018. Herbivory-responsive calmodulin-like protein CML9 does not guide jasmonate-mediated defenses in Arabidopsis thaliana. PLoS One. 16;13(5):e0197633. []


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.[…]

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. […] 257, 37–47.

Zhu X, Robe E, Jomat L, Aldon A, Mazars C, Galaud JP (2017) Calmodulin-like 8 contributes to plant immunity.[…] 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.

Badet T*, Peyraud R*, Mbengue M*, Navaud O, Derbyshire M, Oliver RP, Barbacci A, Raffaele S (2017) Codon optimization underpins generalist parasitism in fungi. Elife

Badet T, Voisin D, Mbengue M, Barascud M, Sucher J, Sadon P, Balague C, Roby D, Raffaele S (2017) Parallel evolution of the POQR prolyl oligo peptidase gene conferring plant quantitative disease resistance. PLoS Genet 13: e1007143

Bucherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M, Robatzek S, MacLean D, Ott T, Zipfel C (2017) Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. Elife 6

Derbyshire M, Denton-Giles M, Hegedus D, Seifbarghy S, Rollins J, van Kan J, Seidl MF, Faino L, Mbengue M, Navaud O, Raffaele S, Hammond-Kosack K, Heard S, Oliver R (2017) The complete genome sequence of the phytopathogenic fungus Sclerotinia sclerotiorum reveals insights into the genome architecture of broad host range pathogens. Genome Biol Evol 9: 593-618


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

Mbengue M*, Bourdais G*, Gervasi F, Beck M, Zhou J, Spallek T, Bartels S, Boller T, Ueda T, Kuhn H, Robatzek S (2016) Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases. Proc Natl Acad Sci U S A 113: 11034-11039

Mbengue M, Navaud O, Peyraud R, Barascud M, Badet T, Vincent R, Barbacci A, Raffaele S (2016) Emerging Trends in Molecular Interactions between Plants and the Broad Host Range Fungal Pathogens Botrytis cinerea and Sclerotinia sclerotiorum. Front Plant Sci 7: 422

Mithoe SC, Ludwig C, Pel MJ, Cucinotta M, Casartelli A, Mbengue M, Sklenar J, Derbyshire P, Robatzek S, Pieterse CM, Aebersold R, Menke FL (2016) Attenuation of pattern recognition receptor signaling is mediated by a MAP kinase kinase kinase. EMBO Rep 17: 441-454

Postma J, Liebrand TW, Bi G, Evrard A, Bye RR, Mbengue M, Kuhn H, Joosten MH, Robatzek S (2016) Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol 210: 627-642

Vernie T, Camut S, Camps C, Rembliere C, de Carvalho-Niebel F, Mbengue M, Timmers T, Gasciolli V, Thompson R, le Signor C, Lefebvre B, Cullimore J, Herve C (2016) PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula. Plant Physiol 170: 2312-2324


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


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


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.


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.


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


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


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


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


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


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


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


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


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


PhD students

Julie Mazard
(2018-2021) Role de la proteine de signalisation du calcium CML8 dans la reponse d’Arabidopsis thaliana à de multiples stress: implication dans l’immunité contre plusieurs pathogenes et importance de l’auxine.

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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