GOLVEN peptides regulate lateral root spacing as part of a negative feedback loop on the establishment of auxin maxima

Abstract

The initiation of lateral roots in Arabidopsis requires the accumulation of auxin in lateral root founder cells, yielding a local auxin maximum. The positioning of these auxin maxima along the primary root determines the density and spacing of lateral roots. The GOLVEN6 (GLV6) and GLV10 signaling peptides and their receptors have been established as regulators of lateral root spacing via an inhibitory effect on lateral root initiation. However, it remained unclear how these GLV peptides interfere with auxin signaling or homeostasis. Here we show that GLV6/10 signaling regulates the expression of a subset of auxin response genes during lateral root initiation, downstream of the canonical auxin signaling pathway, while simultaneously inhibiting the establishment of auxin maxima in xylem-pole pericycle cells. We present genetic evidence that this inhibitory effect relies on the activity of the PIN3 and PIN7 auxin export proteins. Furthermore, GLV6/10 peptide signaling was found to enhance PIN7 abundance in the plasma membrane of xylem-pole pericycle cells, which likely stimulates auxin efflux from these cells. Based on these findings, we propose a model in which the GLV6/10 signaling pathway serves as a negative feedback loop that contributes to the robust patterning of auxin maxima along the primary root.