Dissecting the pathways coordinating patterning and growth by plant boundary domains

International audienceBoundary domains play important roles during morphogenesis in plants and animals, but how they contribute to patterning and growth coordination in plants is not understood. The CUC genes determine the boundary domains in the aerial part of the plants and, in particular, they have a conserved role in regulating leaf complexity across Angiosperms. Here, we used tooth formation at the Arabidopsis leaf margin controlled by the CUC2 transcription factor to untangle intertwined events during boundary-controlled morphogenesis in plants. Combining conditional restoration of CUC2 function with morphometrics as well as quantification of gene expression and hormone signaling, we first established that tooth morphogenesis involves a patterning phase and a growth phase. These phases can be separated, as patterning requires CUC2 while growth can occur independently of CUC2. Next, we show that CUC2 acts as a trigger to promote growth through the activation of three functional relays. In particular, we show that KLUH acts downstream of CUC2 to modulate auxin response and that expressing KLUH can compensate for deficient CUC2 expression during tooth growth. Together, we reveal a genetic and molecular network that allows coordination of patterning and growth by CUC2-defined boundaries during morphogenesis at the leaf margin. Author summary During organogenesis, patterning, the definition of functional subdomains, has to be strictly coordinated with growth. How this is achieved is still an open question. In plants, boundary domains are established between neighboring outgrowing structures and play a role not only in the separation of these structures but also in their formation. To further understand how these boundary domains control morphogenesis, we used as a model system the formation of small teeth along the leaf margin of Arabidopsis, which is controlled by the CUP-SHAPED COTYLEDON2 (CUC2) boundary gene. The CUC genes determine the boundary domains in the aerial part of the plants and in particular they have been shown to have a conserved role in regulating serration and leaflet formation across Angiosperms and thus are at the root of patterning in diverse leaf types. We manipulated the expression of this gene using an inducible gene expression that allowed restoration of CUC2 expression in its own domain at different developmental stages and for different durations, and followed the effects on patterning and growth. Thus, we showed that while CUC2 is required for patterning it is dispensable for sustained growth of the teeth, acting as a trigger for growth by the activation of several functional relays. We further showed that these findings are not specific to the inducible restoration of CUC2 function by analyzing multiple mutants