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

Abstract

Lateral root initiation requires the accumulation of auxin in lateral root founder cells, yielding a local auxin maximum. The positioning of 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 their inhibitory effect on lateral root initiation in Arabidopsis. 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, downstream of the canonical auxin signaling pathway, while simultaneously inhibiting the establishment of auxin maxima within xylem-pole pericycle cells that neighbor lateral root initiation sites. 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 membranes 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 mechanism that contributes to the robust patterning of auxin maxima along the primary root.

Sulfated peptides and their receptors: Key regulators of plant development and stress adaptation

“…Auxin accumulates locally during lateral root initiation and development. In vitro treatments with GLVs/RGFs can markedly reduce lateral root formation by preventing auxin accumulation during lateral root initiation ( Jourquin et al., 2023 ). PUCHI , a transcription factor that negatively regulates lateral root development ( Hirota et al., 2007 ; Kang et al., 2013 ), is controlled by RGFs.…”

“…Consistent with this finding, RGF1 treatment cannot alter lateral root numbers in the puchi-1 mutant ( Jeon et al., 2023 ). RGFs were also found to regulate the activities of the auxin efflux proteins PIN3 and PIN7 ( Jourquin et al., 2023 ). RGF1 plays a role in plant gravitropic responses ( Figure 3 D).…”

“…Exogenous treatment with RGF1 was shown to upregulate the phosphorylation of PIN2. However, it remains unclear whether RGFs also induce the phosphorylation of other PINs like PIN3 and PIN7 during lateral root development ( Jourquin et al., 2023 ; Xu et al., 2023 ). In addition, the transcript level of RITF1 is regulated by RGF1 during RGF signal transduction, but it is not yet clear whether this regulation occurs via the known YODA–MKK4/5–MPK3/6 pathway.…”

A Multitrait Genome-Wide Association Study Reveals a Requirement for the Strigolactone Receptor MtDWARF14 in Optimal GOLVEN Signaling

“…The sulfated GLV/RGF family of peptides plays an important role in nodulation controlling nodule number, density, noduletaxis, nodule zone length and, several root architecture traits including primary root length, lateral root density (Fernandez et al, 2015; Fernandez et al, 2020; Li et al, 2020; Jourquin et al, 2022; Roy et al, 2024). Importantly, GOLVEN peptide-coding genes transcriptionally regulated by auxin, and in turn, modulate both nodulation and root architectural traits through interference with auxin accumulation and signaling pathways, pointing at the existence of a feedback loop (Whitford et al, 2012; Jourquin et al, 2023; Roy et al, 2024). Approximately 30% of genes controlled by GLV10 transcriptionally are also regulated by auxin, including auxin efflux transporters PINs and PIN-LIKEs (Roy et al, 2024).…”