Connective auxin transport contributes to strigolactone-mediated shoot branching control independent of the transcription factor BRC1

The shoot systems of plants are built by the action of the primary shoot apical meristem, established during embryogenesis. In the axil of each leaf produced by the primary meristem, secondary axillary shoot apical meristems are established. The dynamic regulation of the activity of these axillary meristems gives shoot systems their extraordinary plasticity of form. The ability of plants to activate or repress these axillary meristems appropriately requires communication between meristems that is environmentally sensitive. The transport network of the plant hormone auxin has long been implicated as a central player in this tuneable communication system, with other systemically mobile hormones, such as strigolactone and cytokinin, acting in part by modulating auxin transport. Until recently, the polar auxin transport stream, which provides a high conductance auxin transport route down stems dominated by the auxin export protein PIN-FORMED1 (PIN1), has been the focus for understanding long range auxin transport in the shoot. However, recently additional auxin exporters with important roles in the shoot have been identified, including PIN3, PIN4 and PIN7. These proteins contribute to a wider less polar stem auxin transport regime, which we have termed connective auxin transport (CAT), because of its role in communication across the shoot system. Here we present a genetic analysis of the role of CAT in shoot branching. We demonstrate that in Arabidopsis, CAT plays an important role in strigolactone-mediated shoot branching control, with the triple pin3pin4pin7 mutant able to suppress partially the highly branched phenotype of strigolactone deficient mutants. In contrast, the branchy phenotype of mutants lacking the axillary meristem-expressed transcription factor, BRANCHED1 (BRC1) is unaffected by pin3pin4pin7. We further demonstrate that mutation in the ABCB19 auxin export protein, which like PIN3 PIN4 and PIN7 is widely expressed in stems, has very different effects, implicating ABCB19 in auxin loading at axillary bud apices. Author summary The plant shoot system can be considered as a population of communicating growing tips, each driven by a shoot apical meristem. Communication between these meristems acts to mediate decisions about which meristems should be active and which dormant, depending on local and systemic environmental information, and hence how branchy a plant becomes. Here we analyse the role of transporters for the plant hormone auxin in this communication network and its ability to make meristem activity decisions. Previous work in this area has focussed on the auxin export protein PIN-FORMED1 (PIN1), which has a relatively narrow expression pattern in stems and is important for high conductance transport of auxin down toward the root. Here we analyse the unique contributions of more widely expressed auxin exporters, namely PIN3 PIN4 and PIN7, as well as ABCB19. We demonstrate that they have distinct roles in regulating axillary meristem activity. PIN3 PIN4 and PIN7 are likely important for communication between the axillary meristems and the main stem PIN1-dominated polar auxin transport stream. In contrast, our results suggest a role for ABCB19 in auxin loading at axillary shoot apices.