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Hormonal Signalling and Development

Personnel du RDP


(33) 4 72 72 89 82

BRUNOUD Géraldine

(33) 4 72 72 86 04


(33) 4 72 72 XX XX

Chen wenqian

(33) 4 72 72 XX XX


(33) 4 72 72 89 82



Thesis ENS


(33) 4 72 72 86 14
Postdoc CNRS

LAINE Stéphanie

(33) 4 72 72 86 03

LEGRAND Jonathan

(33)4 72 72 86 04


(33) 4 72 72 86 06

SHI Bihai

(33) 4 72 72 86 14
Postdoc ANR


(33) 4 72 72 86 01


(33) 4 72 72 XX XX


Galvan-Ampudia CS, Cerutti G, Legrand J, Brunoud G, Martin-Arevalillo R, Azais R, Bayle V, Moussu S, Wenzl C, Jaillais Y, Lohmann JU, Godin C, Vernoux T. "Temporal integration of auxin information for the regulation of patterning.". Elife 9:e55832 (2020)
PMID: 32379043

Fabrice Besnard, Joao Picao-Osorio, Clément Dubois, Marie-Anne Félix "A broad mutational target explains a fast rate of phenotypic evolution". eLife (2020)

Elsa Véron, Teva Vernoux, Yoan Coudert "Phyllotaxis from a Single Apical Cell". Trends in Plant Science Elsevier (2020)

Jekaterina Truskina, Jingyi Han, Elina Chrysanthou, Carlos S. Galvan-Ampudia, Stéphanie Lainé, Géraldine Brunoud, Julien Macé, Simon Bellows, Jonathan Legrand, Anne-Maarit Bågman, Margot E. Smit, Ondřej Smetana, Arnaud Stigliani, Silvana Porco, Malcolm J. Bennett, Ari Pekka Mähönen, François Parcy, Etienne Farcot, Francois Roudier, Siobhan M. Brady, Anthony Bishopp & Teva Vernoux "A network of transcriptional repressors modulates auxin responses". Nature (2020)

Jekaterina Truskina, Jingyi Han, Elina Chrysanthou, Carlos S. Galvan-Ampudia, Stéphanie Lainé, Géraldine Brunoud, Julien Macé, Simon Bellows, Jonathan Legrand, Anne-Maarit Bågman, Margot E. Smit, Ondřej Smetana, Arnaud Stigliani, Silvana Porco, Malcolm J. Bennett, Ari Pekka Mähönen, François Parcy, Etienne Farcot, Francois Roudier, Siobhan M. Brady, Anthony Bishopp & Teva Vernoux. "A network of transcriptional repressors modulates auxin responses.". Nature (2020)


Maugarny-Calès A, Cortizo M, Adroher B, Borrega N, Gonçalves B, Brunoud G, Vernoux T, Arnaud N, Laufs P. "Dissecting the pathways coordinating patterning and growth by plant boundary domains.". PLoS Genetics 1 (2019)
PMID: 30677017

Yoan Coudert, Ondrej Novak, C. Jill Harrison "A KNOX-Cytokinin Regulatory Module Predates the Origin of Indeterminate Vascular Plants". Current Biology 29 1-8 Cell Press (2019)

Coudert Y, Harris S, Charrier B. "Design Principles of Branching Morphogenesis in Filamentous Organisms". Current biology 29 Elsevier (2019)

Delaux PM, Hetherington AJ, Coudert Y, Delwiche C, Dunand C, Gould S, Kenrick P, Li FW, Philippe H, Rensing SA, Rich M, Strullu-Derrien C, de Vries J. "Reconstructing trait evolution in plant evo-devo studies". Current biology 29 Elsevier (2019)


Moody LA, Kelly S, Coudert Y, Nimchuk ZL, Harrison CJ, Langdale JA. "Somatic hybridization provides segregating populations for the identification of causative mutations in sterile mutants of the moss Physcomitrella patens.". New Phytologist 3 (2018)
PMID: 29498048

Lopez-Obando M, de Villiers R, Hoffmann B, Ma L, de Saint Germain A, Kossmann J, Coudert Y, Harrison CJ, Rameau C, Hills P, Bonhomme S. "Physcomitrella patens MAX2 characterization suggests an ancient role for this F-box protein in photomorphogenesis rather than strigolactone signalling". New Phytologist 2 (2018)
PMID: 29781136

Stigliani A, Martin-Arevalillo R, Lucas J, Bessy A, Vinos-Poyo T, Mironova V, Vernoux T, Dumas R, Parcy F. "Capturing Auxin Response Factors Syntax Using DNA Binding Models". Molecular Plant Cell Press (2018)
PMID: 30336329

Raymond O, Gouzy J, Just J, Badouin H, Verdenaud M, Lemainque A, Vergne P, Moja S, Choisne N, Pont C, Carrère S, Caissard JC, Couloux A, Cottret L, Aury JM, Szécsi J, Latrasse D, Madoui MA, François L, Fu X, Yang SH, Dubois A, Piola F, Larrieu A, Perez M, Labadie K, Perrier L, Govetto B, Labrousse Y, Villand P, Bardoux C, Boltz V, Lopez-Roques C, Heitzler P, Vernoux T, Vandenbussche M, Quesneville H, Boualem A, Bendahmane A, Liu C, Le Bris M, Salse J, Baudino S, Benhamed M, Wincker P, Bendahmane M. "The Rosa genome provides new insights into the domestication of modern roses.". Nature Genetics 6 772-777 (2018)
PMID: 29713014

Orosa-Puente B, Leftley N, von Wangenheim D, Banda J, Srivastava AK, Hill K, Truskina J, Bhosale R, Morris E, Srivastava M, Kümpers B, Goh T, Fukaki H, Vermeer JEM, Vernoux T, Dinneny JR, French AP, Bishopp A, Sadanandom A, Bennett MJ. "Root branching toward water involves posttranslational modification of transcription factor ARF7.". Science 6421 1407-1410 (2018)
PMID: 30573626

Armezzani A, Abad U, Ali O, Andres Robin A, Vachez L, Larrieu A, Mellerowicz EJ, Taconnat L, Battu V, Stanislas T, Liu M, Vernoux T, Traas J, Sassi M. "Transcriptional induction of cell wall remodelling genes is coupled to microtubule-driven growth isotropy at the shoot apex in Arabidopsis.". Development (2018)
PMID: 29739839

Shin JH, Mila I, Liu M, Rodrigues MA, Vernoux T, Pirrello J, Bouzayen M. "The RIN-regulated Small Auxin-Up RNA SAUR69 is involved in the unripe-to-ripe phase transition of tomato fruit via enhancement of the sensitivity to ethylene.". New Phytologist 820-836 (2018)
PMID: 30511456

Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R, Truskina J, Leftley N, Hanlon M, Swarup K, Rashed A, Voß U, Alonso J, Stepanova A, Yun J, Ljung K, Brown KM, Lynch JP, Dolan L, Vernoux T, Bishopp A, Wells D, von Wirén N, Bennett MJ, Swarup R. "A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate.". Nature Communications (2018)
PMID: 29651114

Reeb C, Kaandorp J, Jansson F, Puillandre N, Dubuisson JY, Cornette R, Jabbour F, Coudert Y, Patiño J, Flot JF, Vanderpoorten A. "Quantification of complex modular architecture in plants". New Phytologist 2 (2018)
PMID: 29468683

Verger S*, Cerutti G, Hamant O "An Image Analysis Pipeline to Quantify Emerging Cracks in Materials or Adhesion Defects in Living Tissues". Bio Protoc. 8(19):e3036 (2018)
PMID: 30406157

Armezzani A, Abad U, Ali O, Andres Robin A, Vachez L, Larrieu A, Mellerowicz EJ, Taconnat L, Battu V, Stanislas T, Liu M, Vernoux T, Traas J*, Sassi M "Transcriptional induction of cell wall remodelling genes is coupled to microtubule-driven growth isotropy at the shoot apex in Arabidopsis". Development 145(11) (2018)
PMID: 29739839

Stanislas T, Platre MP, Liu M, Rambaud-Lavigne LES, Jaillais Y, Hamant O* "A phosphoinositide map at the shoot apical meristem in Arabidopsis thaliana". BMC Biol. 16(1):20 (2018)
PMID: 29415713


Besnard, F., Koutsovoulos, G., Dieudonné, S., Blaxter, M., and Félix, M.-A. "Toward Universal Forward Genetics: Using a Draft Genome Sequence of the Nematode Oscheius tipulae To Identify Mutations Affecting Vulva Development.". Genetics 206, 1747–1761. (2017)

Vernoux T & Robert S "Auxin 2016: A burst of auxin in the warmth south of China". Development 533-540 (2017)

Martin-Arevalillo R, Nanao MH, Larrieu A, Vinos-Poyo T, Mast D, Galvan-Ampudia C, Brunoud G, Vernoux T, Dumas R, Parcy F. "The structure of the Arabidopsis TOPLESS corepressor provides insight into the evolution of transcriptional repression". Proceedings of the National Academy of Sciences 30 8107-8112 (2017)
PMID: 28698367

Coudert Y, Bell NE, Edelin C & Harrison CJ "Multiple innovations underpinned branching form diversification in mosses". New Phytologist 2 840-850 (2017)
PMID: 28470778

Truskina J, Vernoux T "The growth of a stable stationary structure: coordinating cell behavior and patterning at the shoot apical meristem". Current Opinion in Plant Biology 41 83-88 (2017)

Coudert Y. "The evolution of branching in land plants: between conservation and diversity". Evolutionary Developmental Biology. Springer, Cham (2017)
Evolutionary Developmental Biology - A Reference Guide, L. Nuño de la Rosa, G.B. Müller


Lauxmann M. A., Annunziata M. G., Brunoud G., Wahl V., Koczut A., Burgos A., Olas J.J., Maximova E., Abel C., Schlereth A., Soja A.M., Bläsing O.E. and Lunn J.E. and Vernoux T., & Stitt M. "Reproductive failure in Arabidopsis thaliana under transient carbohydrate limitation: Flowers and very young siliques are jettisoned and the meristem is maintained to allow successful resumption of reproductive growth". Plant, Cell and Environment 4 745-767 (2016)

Legrand J., Léger J.-B., Robin S., Vernoux T. & Guédon Y. "Modelling the influence of dimerisation sequence dissimilarities on the auxin signalling network". BMC Systems Biology 1 (2016)

Parcy F., Vernoux T. & Dumas R. "A Glimpse beyond Structures in Auxin-Dependent Transcription". Trends in Plant Science 7 574–583 (2016)

Galvan-Ampudia C. S., Chaumeret A. M., Godin C. & Vernoux T. "Phyllotaxis: from patterns of organogenesis at the meristem to shoot architecture". Wiley Interdisciplinary Reviews: Developmental Biology 5 460-473 (2016)

Refahi, Y., Brunoud, G., Farcot, E., Jean-Marie, A., Pulkkinen, M., Vernoux, T., & Godin, C. "A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis". eLife 5 231–244 (2016)
Featured in Labtimes (p. 34-35), CNRS national website, ENS Lyon website.

Larrieu, A., & Vernoux, T. "Q&A: How does jasmonate signaling enable plants to adapt and survive?". BMC Biology 1 79 (2016)


Landrein B, Refahi Y, Besnard F, Hervieux N, Mirabet V, Boudaoud A, Vernoux T, Hamant O. "Meristem size contributes to the robustness of phyllotaxis in Arabidopsis.". Journal of Experimental Botany 66 1317-24 (2015)
PMID: 25504644

Larrieu A., Champion A., Legrand J., Lavenus J., Mast D., Brunoud G., Oh J., Guyomarc’h S., Pizot M., Farmer E.E., Turnbull C., Vernoux T.*, Bennett M.*, & Laplaze L.* "A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants". Nature Communications 6 (2015)
Featured in Nature Plants, Science & Avenir (French science magazine for general public), Le Monde (Blog Passeur de Sciences), Libération (Blog Sciences2) and CNRS, INRA, ENS Lyon and Nottingham University websites

Liao, C.-Y., Smet, W., Brunoud, G., Yoshida, S., Vernoux, T., & Weijers, D. "Reporters for sensitive and quantitative measurement of auxin response". Nature Methods 3 207-210 (2015)

Larrieu, A., & Vernoux, T. "Comparison of plant hormone signalling systems". Essays in Biochemistry 165-181 (2015)

Farcot E, Lavedrine C, & Vernoux T "A modular analysis of the auxin signalling network". PLoS ONE 10 (2015)
PMID: 25807071

Colling, J., Tohge, T., De Clercq, R., Brunoud, G., Vernoux, T., Fernie, A. R., Makunga, N.P., Goossens, A., & Pauwels, L. "Overexpression of the Arabidopsis thaliana signalling peptide TAXIMIN1 affects lateral organ development". Journal of Experimental Botany 66 5337–5349 (2015)

Lavedrine, C., Farcot, E., & Vernoux, T. "Modeling plant development: From signals to gene networks". Current Opinion in Plant Biology 148–153 (2015)
PMID: 26247125

Cerutti, G., Ribes, S., Godin, C., Galvan-Ampudia, C., & Vernoux, T. "3-d Tessellation of Plant Tissue-A Dual Optimization Approach to Cell-Level Meristem Reconstruction from Microscopy Images". IEEE - 2015 International Conference on 3D Vision 443–451 (2015)

Moreno-Risueno, M. A., Sozzani, R., Yardımcı, G. G., Petricka, J. J., Vernoux, T., Blilou, I., Alonso, J., Winter, C.M., Ohler, U., Scheres, B., & Benfey, P. N. "Transcriptional control of tissue formation throughout root development". Science 6259 426–30 (2015)

Landrein B, Kiss A, Sassi M, Chauvet A, Das P, Cortizo M, Laufs P, Takeda S, Aida M, Traas J, Vernoux T, Boudaoud A, Hamant O. "Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems.". Elife 4 (2015)
PMID: 26623515
Featured in F1000 (2★)


Sassi M, Ali O, Boudon F, Cloarec G, Abad U, Cellier C, Chen X, Gilles B, Milani P, Friml J, Vernoux T, Godin C, Hamant O, Traas J "An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis". Curr Biol. 24(19):2335-42 (2014)
PMID: 25264254

Landrein B, Vernoux T "Auxin, chief architect of the shoot Apex". Auxin and its role in plant development pp 191-212 Zazimalova et al., eds (Springer-Verlag Wien) (2014)
Besnard, F., Refahi, Y., Morin, V., Marteaux, B., Brunoud, G., Chambrier, P., Rozier F., Mirabet V., Legrand J., Lainé S., Thévenon E., Farcot E., Cellier C., Das P., Bishopp A., Dumas R., Parcy F., Helariutta Y., Boudaoud A., Godin C., Traas J., Guédon Y., & Vernoux, T. "Cytokinin signalling inhibitory fields provide robustness to phyllotaxis.". Nature. 505 417-21 (2014)
PMID: 24336201
Featured in F1000 (2★)

Galvan-Ampudia, C. S., & Vernoux, T. "Signal integration by GSK3 kinases in the root". Nature Cell Biology 1 21-23 (2014)

Band, L. R., Wells, D. M., Fozard, J. A., Ghetiu, T., French, A. P., Pound, M. P., Wilson M. H., Yu L., Li W., Hijazi H.I., Oh J., Pearce S.P., Perez-Amador M.A., Yun J., Kramer E., Alonso J.M., Godin C., Vernoux T., Hodgman T.C., Pridmore T.P., Swarup R., King J.R., & Bennett, M. J "Systems analysis of auxin transport in the Arabidopsis root apex". Plant Cell 3 862–875 (2014)
Featured in F1000 (2★)

Nanao, M. H., Vinos-Poyo, T., Brunoud, G., Thévenon, E., Mazzoleni, M., Mast, D., Lainé S., Wang S., Hagen G., Li H., Guilfoyle T.J., Parcy F., Vernoux T., & Dumas, R. "Structural basis for oligomerization of auxin transcriptional regulators". Nature Communications 5 (2014)
PMID: 24710426
Featured in F1000 (2★)

Besnard F., Rozier F., & Vernoux T. "The AHP6 cytokinin signaling inhibitor mediates an auxin-cytokinin crosstalk that regulates the timing of organ initiation at the shoot apical meristem". Plant Signaling & Behavior 9 4-7 (2014)

Wang, Q., Kohlen, W., Rossmann, S., Vernoux, T., & Theres, K. "Auxin Depletion from the Leaf Axil Conditions Competence for Axillary Meristem Formation in Arabidopsis and Tomato". Plant Cell 5 2068–2079 (2014)
Featured in F1000 (2★)

Bao, Y., Aggarwal, P., Robbins, N. E., Sturrock, C. J., Thompson, M. C., Tan, H. Q., Tham C., Duan L., Rodriguez P.L., Vernoux T., Mooney S.J., Bennett M.J. & Dinneny, J. R. "Plant roots use a patterning mechanism to position lateral root branches toward available water". Proceedings of the National Academy of Sciences of the United States of America 25 9319–24 (2014)
Featured in F1000 (3★)

Rozier, F., Mirabet, V., Vernoux, T., & Das, P. "Analysis of 3D gene expression patterns in plants using whole-mount RNA in situ hybridization". Nature Protocols 10 2464-2475 (2014)

Sassi, M., Ali, O., Boudon, F., Cloarec, G., Abad, U., Cellier, C., Milani P., Chen X., Friml J., Vernoux T., Godin C., Hamant O., & Traas, J. "An Auxin-Mediated Shift toward Growth Isotropy Promotes Organ Formation at the Shoot Meristem in Arabidopsis". Current Biology 19 2335-2342 (2014)

Hohm, T., Demarsy, E., Quan, C., Allenbach Petrolati, L., Preuten, T., Vernoux, T., Bergmann S., & Fankhauser, C. "Plasma membrane H+ -ATPase regulation is required for auxin gradient formation preceding phototropic growth". Molecular Systems Biology 9 751 (2014)

Qi, J., Wang, Y., Yu, T., Cunha, A., Wu, B., Vernoux, T., Meyerowitz E.M., & Jiao, Y. "Auxin depletion from leaf primordia contributes to organ patterning". Proceedings of the National Academy of Sciences 52 18769–18774 (2014)


Wells, D. M., Laplaze, L., Bennett, M. J., & Vernoux, T. "Biosensors for phytohormone quantification: Challenges, solutions, and opportunities". Trends in Plant Science 5 244-249 (2013)

Sassi, M., Wang, J., Ruberti, I., Vernoux, T., & Xu, J. "Shedding light on auxin movement: light-regulation of polar auxin transport in the photocontrol of plant development". Plant Signaling & Behavior 3 (2013)

Sassi, M., & Vernoux, T. "Auxin and self-organization at the shoot apical meristem". Journal of Experimental Botany 9 2579-2592 (2013)

Oliva, M., Farcot, E., & Vernoux, T. "Plant hormone signaling during development: insights from computational models". Current Opinion in Plant Biology 1 19-24 (2013)
Guédon, Y., Refahi, Y., Besnard, F., Farcot, E., Godin, C., & Vernoux, T. "Pattern identification and characterization reveal permutations of organs as a key genetically controlled property of post-meristematic phyllotaxis". Journal of Theoretical Biology 338 94-110 (2013)

Galvan-Ampudia, C. S., Julkowska, M. M., Darwish, E., Gandullo, J., Korver, R. A., Brunoud, G., Haring M.A., Munnik T., Vernoux T., & Testerink, C. "Halotropism is a response of plant roots to avoid a saline environment". Current Biology 20 2044-2050 (2013)
Featured in F1000 (9★), Nature Structural and Molecular Biology and The Scientist.


Mirabet, V., Besnard, F., Vernoux, T.*, & Boudaoud, A.* "Noise and robustness in phyllotaxis". PLoS Computational Biology 2 (2012)

Brunoud, G., Wells, D. M., Oliva, M., Larrieu, A., Mirabet, V., Burrow, A. H., Beeckman T., Kepinski S., Traas J., Bennett M.J., Vernoux, T. "A novel sensor to map auxin response and distribution at high spatio-temporal resolution". Nature 103–6 (2012)
Featured in F1000 (14★), Nature Methods, ACS Chemical Biology (p.2), The Scientist.

Band, L. R., Wells, D. M., Larrieu, A., Sun, J., Middleton, A. M., French, A. P., Brunoud G., Sato E.M., Wilson M.H., Peret B., Oliva M., Swarup R., Sairanen I., Parry G., Ljung K., Beeckman T., Garibaldi J.M., Estelle M., Owen M.R., Vissenberg K., Hodgman T.C., Pridmore T.P., King J.R., Vernoux T.*, Bennett M.J.* "Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism". Proceedings of the National Academy of Sciences of the United States of America 12 4668–4673 (2012)
PMID: 22393022

Reymond, M. C., Brunoud, G., Chauvet, A., Martinez-Garcia, J. F., Martin-Magniette, M.-L., Moneger, F., & Scutt, C. P. "A Light-Regulated Genetic Module Was Recruited to Carpel Development in Arabidopsis following a Structural Change to SPATULA". The Plant Cell 7 2812–2825 (2012)

Sassi, M., Lu, Y., Zhang, Y., Wang, J., Dhonukshe, P., Blilou, I., Dai M., Li J., Gong X., Jaillais Y., Yu X., Traas J., Ruberti I., Wang H., Scheres B., Vernoux T.*, & Xu, J.* "COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis". Development 18 3402-12 (2012)

Middleton, A. M., Farcot, E., Owen, M. R., & Vernoux, T. "Modeling Regulatory Networks to Understand Plant Development: Small Is Beautiful". Plant Cell 10 3876–3891 (2012)


Besnard F., Vernoux T., & Hamant O. "Organogenesis from stem cells in planta: Multiple feedback loops integrating molecular and mechanical signals". Cellular and Molecular Life Sciences 17 2885–2906 (2011)

Refahi, Y., Farcot, E., Guédon, Y., Besnard, F., Vernoux, T., & Godin, C. "A Combinatorial Model of Phyllotaxis Perturbations in Arabidopsis thaliana". Lecture Notes in Computer Science 323–335 Springer, Berlin, Heidelberg. (2011)

Vernoux, T., Brunoud, G., Farcot, E., Morin, V., Van den Daele, H., Legrand, J., Oliva M., Das P., Larrieu A., Wells D., Guedon Y., Armitage L., Picard F., Guyomarc'h S., Cellier C., Parry G., Koumproglou R., Doonan J.H., Estelle M., Godin C., Kepinski S., Bennett M., De Veylder L., & Traas, J. "The auxin signalling network translates dynamic input into robust patterning at the shoot apex". Molecular Systems Biology 1 508 (2011)
Featured in F1000 (2★)

Santuari, L., Scacchi, E., Rodriguez-Villalon, A., Salinas, P., Dohmann, E. M. N., Brunoud, G., Vernoux T., Smith R.S., & Hardtke, C. S. "Positional Information by Differential Endocytosis Splits Auxin Response to Drive Arabidopsis Root Meristem Growth". Current Biology 22 1918–1923 (2011)


Vernoux, T., Besnard, F., & Traas, J. "Auxin at the shoot apical meristem". Cold Spring Harbor Perspectives in Biology 4 (2010)

Gaamouche, T., Manes, C.-L. de O., Kwiatkowska, D., Berckmans, B., Koumproglou, R., Maes, S., Beeckman T., Vernoux T., Doonan J.H., Traas J., Inze D., & De Veylder, L. "Cyclin-dependent kinase activity retains the shoot apical meristem cells in an undifferentiated state". The Plant Journal 1 26-37 (2010)

Bashandy, T., Guilleminot, J., Vernoux, T., Caparros-Ruiz, D., Ljung, K., Meyer, Y., & Reichheld, J.-P. "Interplay between the NADP-Linked Thioredoxin and Glutathione Systems in Arabidopsis Auxin Signaling". Plant Cell 2 376–391 (2010)
(2010). . The Plant Cell, 22(2), 376–391.

De Rybel, B., Vassileva, V., Parizot, B., Demeulenaere, M., Grunewald, W., Audenaert, D., Van Campenhout J., Overvoorde P., Jansen L., Vanneste S., Moller B., Wilson M., Holman T., Van Isterdael G., Brunoud G., Vuylsteke M., Vernoux T., De Veylder L., Inze D., Weijers D., Bennett M.J., & Beeckman, T. "A Novel Aux/IAA28 Signaling Cascade Activates GATA23-Dependent Specification of Lateral Root Founder Cell Identity". Current Biology 19 1697–1706 (2010)

Traas, J., & Vernoux, T. "Oscillating Roots". Science 5997 1290–1291 (2010)

Sozzani, R., Cui, H., Moreno-Risueno, M. a, Busch, W., Van Norman, J. M., Vernoux, T., Brady S.M., Dewitte W., Murray J.A., & Benfey, P. N. "Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth". Nature 7302 128–132 (2010)


Das P, Ito T, Wellmer F, Vernoux T, Dedieu A, Traas J, Meyerowitz EM "Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA". Development 10 1605-1611 (2009)
PMID: 19395638


Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P "Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome". Theoretical and Applied Genetics 3 473-486 (2007)
PMID: 17136373

Cui H, Levesque MP*, Vernoux T*, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN "An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants". Science 421-425 (2007)
PMID: 17446396
* co-2nd author
Featured in F1000 (6: Exceptional)


Levesque MP*, Vernoux T*, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN "Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis". PLoS Biology 5 (2006)
PMID: 16640459
* co-1st author
Featured in F1000 (4: Exceptional)


Vernoux T, Benfey PN "Signals that regulate stem cell activity during plant development". Current Opinion in Genetics & Development 4 388-394 (2005)
PMID: 15967658


Guyomarc'h S, Vernoux T, Traas J, Zhou DX, Delarue M "MGOUN3, an Arabidopsis gene with TetratricoPeptide-Repeat-related motifs, regulates meristem cellular organization". Journal of Experimental Botany 397 673-684 (2004)
PMID: 14966212

Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M "PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis". Development 20 5021-5030 (2004)
PMID: 15371311

Grandjean O, Vernoux T, Laufs P, Belcram K, Mizukami Y, Traas J "In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis". Plant Cell 1 74-87 (2004)
PMID: 14671026
Featured in F1000 (4: Exceptional)


Traas J, Vernoux T. "The shoot apical meristem: the dynamics of a stable structure". Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 1422 737-747 (2002)
PMID: 12079669

Aida M*, Vernoux T*, Furutani M, Traas J, Tasaka M "Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo". Development 17 3965-3974 (2002)
PMID: 12163400
* co-1st author


Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inze D, May MJ, Sung ZR "The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development". Plan Cell 1 97-110 (2000)
PMID: 10634910

Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J " PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem". Development 23 5157-5165 (2000)
PMID: 11060241
(2000b). 127: 5157-5165.

Vernoux T, Autran D, Traas J "Developmental control of cell division patterns in the shoot apex". Plant Molecular Biology 5-6 569-581 (2000)
PMID: 11089861


Reichheld J-P, Vernoux T, Lardon F, Van Montagu M, Inzé D "Specific checkpoints regulate plant cell cycle progression in response to oxidative stress". The Plant Journal 6 647-656 (1999)


May MJ, Vernoux T, Leaver C, Montagu MV, Inzé D "Glutathione homeostasis in plants: implications for environmental sensing and plant development". Journal of Experimental Botany 321 649-667 (1998)

May MJ, Vernoux T, Sanchez-Fernandez R, Van Montagu M, Inze D "Evidence for posttranscriptional activation of gamma-glutamylcysteine synthetase during plant stress responses". PNAS 20 12049-12054 (1998)
PMID: 9751788

Scientific context:

From dynamic patterning to global plant architecture

Research in the SIGNAL team addresses a question central to developmental biology: how do non-linear interactions at multiple scales (molecule, cell, tissue, organism) lead to coordinated cell behaviours and to the emergence of precise forms in multi-cellular organisms?
For instance, many of our projects are connected to phyllotaxis, the geometric arrangement of leaves, branches and flowers along stems, which shows striking regularities and puzzling mathematical properties. We use both seed plants and mosses as model systems, and interdisciplinary approaches to tackle this question. To capture how developmental dynamics link genotypes to phenotypes, our approaches are deeply rooted in functional genetics and rely on quantitative phenotyping at all scales (e.g. using confocal imaging), real-time observations and computational modelling.

More specific research themes focus on:
- Hormonal signals and developmental dynamics at the shoot apical meristem
- Genetic control and robustness of inflorescence architecture
- Hormonal control and evolution of branching forms
- Multi-scale imaging solutions for the quantitative analysis of forms


Hormonal signals and developmental dynamics at the shoot apical meristem

Project leader: Teva Vernoux
Persons involved: Géraldine Brunoud (CNRS Research Engineer), Carlos Galván-Ampudia (Senior postdoc), Raquel Martin-Arevalillo (Postdoc), Estefania Pavesi (PhD Student; co-supervisor: Matias Zurbriggen, University of Düsseldorf), Marketa Pernisova (Postdoc), Bihai Shi (Postdoc).

The shoot apical meristem, a specialized tissue containing a stem cell niche, produces new lateral organs throughout the life of the plant. Here, we investigate how spatio-temporal distribution of hormonal signals and hormone signalling activity contribute to reiterative patterning at the shoot apical meristem.

To do so, we follow a number of complementary lines of research aiming to:
- Obtain a quantitative understanding of how the spatio-temporal distribution of auxin is controlled;
- Analyze the gene network controlling the response to auxin in space and time;
- Understand how symplasmic connections contribute to hormone distribution and patterning;
- Understand how hormones act in controlling growth at the shoot apical meristem and how this contributes to the dynamics of patterning;
- Understand the molecular mechanisms allowing auxin to act in cell fate determination;
- Decipher the molecular basis of auxin-cytokinin interactions during organ patterning at the shoot apical meristem.

We use approaches ranging from quantitative imaging, genomics, genetics to synthetic biology and computational modelling.

Main collaborators: Patrick Achard (IPMB Strasbourg), Malcolm Bennett (University of Nottingham), Anthony Bishopp (University of Nottingham), Siobhan Brady (UC Davis), Renaud Dumas (LPCV Grenoble), Christophe Godin (RDP), Jan Lohman (University of Heidelberg), François Parcy (LPCV Grenoble), François Roudier (RDP), Lyuba Ryabova (IPMB Strasbourg), Dolf Weijers (Wagenigen University), Matias Zurbriggen (University of Düsseldorf)

Genetic control and robustness of inflorescence architecture

Project leaders: Fabrice Besnard and Teva Vernoux
Persons involved: Sana Dieudonné (Ph.D Student), Stéphanie Lainé (INRA Research technician)

Here, we aim to identify key genetic mechanisms controlling plant architecture without prior assumptions. First, we are searching for plants from varied genetic backgrounds with altered shoot architecture traits indicating either a perturbation at the shoot apical meristem and/or a change in the robustness of these traits (i.e. where the variance of the trait is modified). Second, we are aiming to identify the genetic basis explaining the altered phenotypes. We expect to discover novel genes or to shed new light on how known genes act in the dynamics of plant developmental systems. When possible, we work with natural genetic variations that allow us to question how generic are the mechanisms found in laboratory lines and how phenotypic changes occur in natural populations and during evolution.

Ongoing projects are:
-  Forward genetics of Arabidopsis thaliana mutants affected in organogenesis and phyllotaxis (S. Laine & F. Besnard / past member: A. Chaumeret)
We are currently investigating a few uncharacterized mutants isolated from Versailles stock center, affected in organogenesis and phyllotaxis. These mutants are in a different genetic background than the widely used Columbia‑0 accession.

-  Natural variation of phyllotaxis robustness (F. Besnard)
Despite its regular nature, we showed that inflorescence phyllotaxis shows substantial variations in different genetic backgrounds. Studying those variations can reveal biological watermarks of phyllotaxis and indicate how cell behaviours are coordinated in space and time to generate phyllotactic patterns. We are currently screening different natural accessions to characterize the perturbation levels of their phyllotaxis.

- Coordination of organ identities during rapid phase transition (S. Dieudonné)
Flowering plants switch rapidly from vegetative to floral states when they start producing flowers. In Brassicaceae, including the model plant Arabidopsis thaliana, shoots stop producing basic units comprising a leaf and a branch to make only flowers. No intermediate forms are produced. Strong evidence indicates that the leaf (also called ’bract’) is suppressed when the flower arises, through yet unclear mechanisms that evolved in Brassicaceae. We identified a genetic background in Arabidopsis in which some bracts are associated with flowers at the floral transition. We are currently characterizing the genetic variations that disturb the robust coordination between bracts and flowers upon the floral transition.

Hormonal control and evolution of branching forms

Project leader: Yoan Coudert
Persons involved: Elsa Véron (PhD student), Stéphanie Laine (INRA Research technician), Moira Courseaux (M2 Student)

A key aim in biology is to understand which developmental and genetic changes contributed to the evolution of form through time. In plants, the varied branching patterns emerging from the coordinated activity of meristems at the shoot tips is a key determinant of shape diversity. Hormonal cues have been shown to play a major role in branching control in distinct plant lineages. Here, we aim to understand (1) how the interplay between hormonal cues regulates branch patterning and (2) how this interplay has been remodelled in evolution to generate architectural diversity in plants. We use mosses as model organisms.

Ongoing projects are:
- Evolution of branching control and meristem function in plants
Branch patterning in the shoot is coordinated at the whole plant level by three hormones: auxin, cytokinin and strigolactone. These molecules existed before the divergence between mosses and vascular plants, and were independently recruited in both plant lineages to control leafy shoot branching. In vascular plants, including Arabidopsis thaliana, long-range auxin transport is mediated by PIN proteins and is a key regulator of branching. In the moss Physcomitrium patens, pharmacological inhibitor and mutant analysis experiments have shown that homologues of PIN genes have only a minor role in shoot branching. Instead, apolar and diffusive auxin transport has been proposed as a novel regulator of branching in moss, and could be mediated by callose-regulated plasmodesmal gating. Our goal is to understand how hormonal cues coordinate branching in the moss Physcomitrium patens .

- Polarity control and shoot development from a single apical cell
Phyllotaxis, the geometry of leaf arrangement around stems, determines plant architecture. Molecular interactions coordinating the formation of phyllotactic patterns have mainly been studied in multicellular shoot apical meristems of flowering plants. Phyllotaxis evolved independently in the major land plant lineages. In mosses, it arises from a single apical cell, raising the question of how the polarity and asymmetric divisions of a single-celled meristem create phyllotactic patterns and whether associated genetic processes are shared across lineages. We use the model moss, Physcomitrium patens, to investigate this fundamental biological problem and identify the mechanisms governing shoot apical cell activity.

Multiscale imaging solutions for the quantitative analysis of forms

Project leaders: Fabrice Besnard, Yoan Coudert, Teva Vernoux
Persons involved: Géraldine Brunoud (CNRS Research Engineer), Julie Charlaix (Engineer), Jonathan Legrand (CNRS Research Engineer), Carlos Galván-Ampudia (Senior postdoc), Bihai Shi (Postdoc)

A limiting factor for understanding the dynamics of shape emergence is the capacity to quantify developmental parameters in time and space at different scales. In order to capture these developmental parameters, the SIGNAL team has been and continue developing:
- Biosensors for hormones;
- Open-source robotic solution to automate the phenotyping of aerial parts of plants (and notably Arabidopsis) with high precision (and reasonable through-put);
- Software solutions for quantitative image analysis.

Main collaborators: Patrick Achard (IPMB Strasbourg), Christophe Godin (RDP), Peter Hannappe (Sony CSL Paris), Jonathan Michin (IAAC Barcelona), Verena Hafner (HU Berlin), Matias Zurbriggen (University of Düsseldorf)

Key publications:

-  Coudert Y, Bell NE, Edelin C, Harrison CJ. Multiple innovations underpinned branching form diversification in mosses. New Phytologist, 10.1111/nph.14553 (2017)

-  Refahi Y, Brunoud G, Farcot E, Jean-Marie A, Pulkkinen M, Vernoux T*, Godin C * (2016). A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis. eLife 5 :e14093

-  Larrieu A, Champion A, Legrand J, Lavenus J, Mast D, Brunoud G, Oh J, Guyomarc’h S, Pizot M, Farmer EE, Turnbull C, Vernoux T*, Bennett M* & Laplaze L* (2015) A novel fluorescent hormone biosensor reveals the dynamics of jasmonate signaling in plants. Nature Communications 6:6043

-  Coudert Y, Palubicki W, Ljung K, Novak O, Leyser O, Harrison CJ. Three ancient hormonal cues coordinate shoot branching in the moss Physcomitrella. eLife, 10.7554/eLife.06808 (2015)

-  Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G., Chambrier P, Rozier F, Mirabet V, Legrand J, Lainé S, Thévenon E, Farcot E, Cellier C, Das P, Bishopp A, Dumas R, Parcy F, Helariutta Y, Boudaoud A, Godin C, Traas J, Guédon, Y, Vernoux T* (2014). Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505, 417–421

-  Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T* (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103-106