A BRC1-modulated switch in auxin efflux accounts for the competition between Arabidopsis axillary buds

As part of their modular development, plants continuously adapt their shoot branching architecture according to environmental conditions. This occurs by regulating the activity of axillary buds established in each leaf axil. Whether a bud grows into a shoot depends partly on the presence of other active shoots, which can inhibit bud activation. This systemic coordination is proposed to be mediated by the transport network of the plant hormone auxin, with buds competing to establish sustained transport of auxin, termed canalized auxin transport, into the main stem. A second hormone, strigolactone, tunes this competition by influencing the removal of the PIN1 auxin export protein from the plasma membrane, and hence the dynamics of canalization. Strigolactone also regulates the expression of another key regulatory hub, the bud-expressed transcription factor BRANCHED1 (BRC1). The interplay between auxin transport and BRC1 in regulating bud activity is poorly understood. Here, we investigate this interplay in the context of competition between buds, using Arabidopsis explants with two axillary buds as a minimal system. Using experimental data, we develop a mathematical model of bud-bud competition in which BRC1 influences the establishment of canalized auxin transport by regulating the basal rate of auxin efflux in buds. We identify single model parameters that plausibly correspond to the dual impact of strigolactone on BRC1 expression and PIN1. We show that modulating these two parameters reproduces the dynamics of bud growth and bud-bud competition observed in relevant mutants and treatments. Our model produces testable hypotheses, which we validate by generating a chimeric PIN1 auxin transporter with impaired strigolactone sensitivity, helping us uncouple the effects of strigolactone on PIN1 and BRC1. These results support the hypothesis that BRC1 influences local bud competitiveness by downregulating the basal rate of auxin efflux in buds. Together with the systemic feedbacks in the auxin transport network, this enables plants to adjust dynamically the number and location of growing branches.