Section: New Results

Regulation of branching mechanisms in plants

Participants : Romain Azaïs, Frédéric Boudon [External Collaborator] , Christophe Godin.

• Research Axes: RA2 (Data-driven models) & RA3 (Plasticity & robustness of forms)

• Key Modelling Challenges: KMC3 (Realistic integrated digital models)

Branching in plants results from the development of apical meristems that recursively produce lateral meristems. These meristems may be more or less differentiated with respect to the apical meristem from which they originate, potentially leading to different types of lateral branches or organs. They also can undergo a more or less long period of inactivation, due to systemic regulation. The understanding of branching systems morphogenesis in plants thus relies on the analysis of the regulatory mechanisms that control both meristem differentiation and inactivation.

Analysis of the diversity of inflorescence architecture in different rice species. Rice is a major cereal for world food security and understanding the genetic and environmental determinants of its branching habits is a timely scientific challenge. The domestication, i.e., the empirical selection by humans, of rice began 10 000 years ago in Asia and 3 000 years ago in Africa. It thus provides a short-term model of the processes of evolution of plants.

Hélène Adam and Stéphane Jouannic from the group Evo-Devo de l'Inflorescence of UMR DIADE at IRD (Montpellier) have collected for years on the different continents an outstanding database of panicle-type inflorescence phenotypes in Asian and African, cultivated and wild, rice species. Classical statistical analysis based on the extraction of characteristic traits for each individual branching system were able to separate wild species from cultivated ones, but could not discriminate between wild species, suggesting that the entire branching structure should be used for classification methods to operate. For this, we are currently developing statistical methods on tree structures (see section 6.3) that should allow us to achieve better discrimination between panicles, based on their branching topology in addition to geometric traits. By coupling the quantitative study of the panicles to genomic analyses carried out by the IRD group, we should be able to highlight which regulation pathways have been selected or altered during the domestication process.

The role of sugars in apical dominance. The outgrowth of axillary buds is a key process in plant branching and which is often shown to be suppressed by the presence of auxin in nodal stems. However, local auxin levels are not always sufficient to explain bud outgrowth inhibition. Recent studies have also identified a contribution of sugar deprivation to this phenomenon. Whether sugars act independently of auxin or other hormones auxin regulates is unknown. Auxin has been shown to induce a decrease of cytokinin levels and to upregulate strigolactone biosynthesis in nodes. Based on rose and pea experiments, both in vitro and in planta, with our collaborators Jessica Bertheloot, Soulaiman Sakr from Institut de Recherche en Horticulture et Semences (IRHS) in Angers, we have shown that sucrose and auxin act antagonistically, dose-dependently, and non-linearly to modulate bud outgrowth. The Angers group provided experimental evidence that sucrose represses bud response to strigolactones but does not markedly affect the action of auxin on cytokinin levels. Using a modeling approach, we tested the ability of this complex regulatory network to explain the observed phenotypes. The computational model can account for various combinations of sucrose and hormones on bud outgrowth in a quantitative manner and makes it possible to express bud outgrowth delay as a simple function of auxin and sucrose levels in the stem. These results provide a simple auxin-sucrose-cytokinin-strigolactone network that accounts for plant adaptation to growing conditions. A paper relating this work is currently under review.

The fractal nature of plants. Inflorescence branching systems are complex and diverse. They result from the interaction between meristem growth and gene regulatory networks that control the flowering transition during morphogenesis. To study these systems, we focused on cauliflower mutants, in which the meristem repeatedly fails in making a complete transition to the flower and for which a complete mechanistic explanation is still lacking.

In collaboration with Eugenio Azpeitia and François Parcy's group in Grenoble, we have developed a first model of the control of floral initiation by genes, refining previous networks from the literature so that they can integrate our hypotheses about the emergence of cauliflower phenotypes. The complete network was validated by multiple analyses, including sensitivity analyses, stable state analysis, mutant analysis, among others. It was then coupled with an architectural model of plant development using L-systems. The coupled model was used to study how changes in gene dynamics and expression could impact in different ways the architectural properties of plants. The model was then used to study how changes in certain parameters could generate different curd morphologies, including the normal and the fractal-like Romanesco. A paper reporting this work is currently being written.