A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana

M. L. Garcia-Gomez (1, 2) , Eugenio Azpeitia (3, 4, 5) , Elena R. Alvarez-Buylla (1, 2)

1 UNAM - Universidad Nacional Autónoma de México = National Autonomous University of Mexico
2 c3 - Centro de Ciencias de la Complejidad
3 VIRTUAL PLANTS - Modeling plant morphogenesis at different scales, from genes to phenotype
4 INRA - Institut National de la Recherche Agronomique
5 Cirad - Centre de Coopération Internationale en Recherche Agronomique pour le Développement

The study of the concerted action of hormones and transcription factors is fundamental to understand cell differentiation and pattern formation during organ development. The root apical meristem of Arabidopsis thaliana is a useful model to address this. It has a stem cell niche near its tip conformed of a quiescent organizer and stem or initial cells around it, then a proliferation domain followed by a transition domain, where cells diminish division rate before transiting to the elongation zone; here, cells grow anisotropically prior to their final differentiation towards the plant base. A minimal model of the gene regulatory network that underlies cellfate specification and patterning at the root stem cell niche was proposed before. In this study, we update and couple such network with both the auxin and cytokinin hormone signaling pathways to address how they collectively give rise to attractors that correspond to the genetic and hormonal activity profiles that are characteristic of different cell types along A. thaliana root apical meristem. We used a Boolean model of the genetic-hormonal regulatory network to integrate known and predicted regulatory interactions into alternative models. Our analyses show that, after adding some putative missing interactions, the model includes the necessary and sufficient components and regulatory interactions to recover attractors characteristic of the root cell types, including the auxin and cytokinin activity profiles that correlate with different cellular behaviors along the root apical meristem. Furthermore, the model predicts the existence of activity configurations that could correspond to the transition domain. The model also provides a possible explanation for apparently paradoxical cellular behaviors in the root meristem. For example, how auxin may induce and at the same time inhibit WOX5 expression. According to the model proposed here the hormonal regulation of WOX5 might depend on the cell type. Our results illustrate how non-linear multi-stable qualitative network models can aid at understanding how transcriptional regulators and hormonal signaling pathways are dynamically coupled and may underlie both the acquisition of cell fate and the emergence of hormonal activity profiles that arise during complex organ development.

Mots clés: arabidopsis thaliana; méristème apical de la racine

Domaines: Biologie végétale

M. L. Garcia-Gomez, Eugenio Azpeitia, Elena R. Alvarez-Buylla. A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana. PLoS Computational Biology, 2017, 13 (4), pp.36. ⟨10.1371/journal.pcbi.1005488⟩. ⟨hal-01607284⟩