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).

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), Jeanne Abitbol-Spangaro (PhD 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

Open access files for publications

Martin-Arevalillo et al., 2025, Cell

You can freely access the accepted version of the Manuscript and to the Main Figures.

Supplementary materials are:

• Supplementary Figures: PDF
• Tables S1 & S5: PDF
• Table S2: XLSX
• Table S3: XLSX
• Table S4: XLSX
• Table S6: XLSX

CC BY-NC-ND - DOI: 10.1016/j.cell.2025.03.028

Fundings: