Environmental strigolactone drives early growth responses to neighboring plants and soil volume in pea.

There has been a dramatic recent increase in the understanding of the mechanisms by which plants detect their neighbors, including by touch, reflected light, volatile organic chemicals, and root exudates. The importance of root exudates remains ill-defined because of confounding experimental variables and difficulties disentangling neighbor detection in shoot and roots. There is evidence that root exudates allow distinction between kin and non-kin neighbors, but identification of specific exudates that function in neighbor detection and/or kin recognition remain elusive. Strigolactones (SLs), which are exuded into the soil in significant quantities in flowering plants to promote recruitment of arbuscular mycorrhizal fungi (AMF), seem intuitive candidates to act as plant-plant signals, since they also act as hormones in plants, with dramatic effects on shoot growth and milder effects on root development. Here, using pea, we test whether SLs act as either cues or signals for neighbor detection. We show that peas detect neighbors early in the life cycle through their root systems, resulting in strong changes in shoot biomass and branching, and that this requires SL biosynthesis. We demonstrate that uptake and detection of SLs exuded by neighboring plants are needed for this early neighbor detection, and that plants that cannot exude SLs are outcompeted by neighboring plants and fail to adjust growth to their soil volume. We conclude that plants both exude SLs as signals to modulate neighbor growth and detect environmental SLs as a cue for neighbor presence; collectively, this allows plants to proactively adjust their shoot growth according to neighbor density.