The emergence of vascular tissues played a central rôle in the plant conquest of land as it enabled plants to improve their capacity to optimize their water resources. Both xylem and phloem were essential for the success of plants in the terrestrial environment, yet little is known about the molecular genetic control of phloem spécification and differentiation. In angiosperms, the dominant group of extant terrestrial plants, phloem is assembled from spécifié conductive cells, the sieve elements. Among the genes involved in vascular tissues formation, OCTOPUS (OPS) operates early during development to promote sieve element differentiation. OPS belongs to a multigenic family represented throughout vascular plants. However, its molecular function and its interaction with other known members of the molecular network controlling protophloem development remain unclear.
Here, with a combination of biochemical, molecular, and genetic approaches, we show that OPS plays a delicate rôle in the interplay between two opposing signaling pathways that détermines cellular commitment to sieve element fate in root meristems of the model plant Arabidopsis thaliana. Our data suggest that OPS is a positive master regulator in this process, that displays an exquisite dosage-sensitive action. Moreover, we show that this gene is highly conserved and already present in the most basai extant angiosperms. We also demonstrate that the activity of OPS protein is in part regulated through the charge at a specific phosphorylation site. Surprisingly, we also show that many highly conserved structural OPS features as well as its peculiar shootward polar subcellular localization are not strictly required for OPS function.
Furthermore, our investigations about OPS interplay with plant hormones signaling pathway, confirmed the previously described its interaction with a negative regulator of brassinosteroid response. However, even though this interaction can amplify OPS activity, it is not essential for its function, suggesting that promoting brassionosteroid signaling by affecting the activity of a negative regulator is likely not the primary output of OPS function. Nevertheless, our data also show a prominent rôle for the protophloem in the médiation of brassinosterpid signaling as limiting the perception of this phytohormone to the protophloem domain only still allows the normal progression of cell division and differentiation at the whole plant level.
In summary, our work not only sheds light on novel molecular features of a master regulator of protophloem development, but also reveals a novel function of vascular tissues in the systemic control of plant development.