Complementary roles for auxin and auxin signalling revealed by reverse engineering lateral root stable prebranch site formation

Teixeira, Joana Santos; Berg, Thea van den; Tusscher, Kirsten ten

doi:10.1242/dev.200927

Cited by 9 publications

(11 citation statements)

References 58 publications

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“…The balance between auxin and GLV6/10 peptide levels, and their spatiotemporal distributions along the pericycle, might thus create inhibitory zones around primordia in which the peptides prevent the initiation of LR primordia in close proximity to pre-existing ones. The importance of such peptide-based lateral inhibition mechanisms was recently highlighted in computational models that simulate how stable and properly spaced pre-branch sites can arise from the periodic priming of LRFCs in the elongation zone (Santos Teixeira et al, 2022). In these models inhibitory peptides were assumed to suppress auxin signaling activity in neighboring XPP cells, but our data indicate that they might also reduce the actual auxin levels within these cells.…”

Section: Discussionmentioning

confidence: 86%

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

Jourquin

Fernandez

Wang

et al. 2023

Journal of Experimental Botany

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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.

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Section: Discussionmentioning

confidence: 86%

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

Jourquin

Fernandez

Wang

et al. 2023

Journal of Experimental Botany

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“…PBS derive from stabilized maxima of the oscillating DR5::LUC signal that can be detected close to the meristem (Moreno‐Risueno et al ., 2010; Santos Teixeira et al ., 2022). Given the increase in PBS, we analyzed DR5::LUC dynamics in the elongation zone in the root tip of different genotypes over 22 h. The oscillation period in gh3hex and dao1‐1/gh3hex was significantly shorter than WT (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Still, here we observed an increase rather than a decrease in PBS density expressed as PBS per unit root length. While this increase in PBS density likely partly arises from an enhanced success rate with which auxin oscillations are translated into PBS (Santos Teixeira et al ., 2022), differences may also arise due to differences in cell size.…”

Section: Resultsmentioning

confidence: 99%

“…This implies that weak auxin oscillations are dissipated and forgotten, while stronger ones are memorized for subsequent formation of a PBS with intense auxin signaling. Modeling work suggests that the amplitude of auxin oscillations depends on overall root tip auxin availability (van den Berg et al ., 2021), and that sufficient oscillation amplitude as well as local auxin biosynthesis contribute to successful PBS formation (Laskowski & ten Tusscher, 2017; Santos Teixeira et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

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GH3‐mediated auxin inactivation attenuates multiple stages of lateral root development

Wang,

De Gernier,

Duan

et al. 2023

New Phytologist

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Summary Lateral root (LR) positioning and development rely on the dynamic interplay between auxin production, transport but also inactivation. Nonetheless, how the latter affects LR organogenesis remains largely uninvestigated. Here, we systematically analyze the impact of the major auxin inactivation pathway defined by GRETCHEN HAGEN3‐type (GH3) auxin conjugating enzymes and DIOXYGENASE FOR AUXIN OXIDATION1 (DAO1) in all stages of LR development using reporters, genetics and inhibitors in Arabidopsis thaliana. Our data demonstrate that the gh3.1/2/3/4/5/6 hextuple (gh3hex) mutants display a higher LR density due to increased LR initiation and faster LR developmental progression, acting epistatically over dao1‐1. Grafting and local inhibitor applications reveal that root and shoot GH3 activities control LR formation. The faster LR development in gh3hex is associated with GH3 expression domains in and around developing LRs. The increase in LR initiation is associated with accelerated auxin response oscillations coinciding with increases in apical meristem size and LR cap cell death rates. Our research reveals how GH3‐mediated auxin inactivation attenuates LR development. Local GH3 expression in LR primordia attenuates development and emergence, whereas GH3 effects on pre‐initiation stages are indirect, by modulating meristem activities that in turn coordinate root growth with LR spacing.

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“…Auxin dynamics were modeled on a two-dimensional cross section of an idealized Arabidopsis thaliana root tip anatomy containing at its distal end a quiescent center, surrounded by stem cell niche, columella, and root cap, and shootward from the QC consisting from inside to outside epidermal, cortical, endodermal, pericycle and multiple vascular tissue cell files. The model incorporates experimentally derived cell type and root zone specific patterns of the AUX/LAX auxin importers, the polarly localized PIN auxin exporters, and in addition to baseline cell level auxin production and degradation elevated levels of auxin production around the QC, in the columella and lateral root cap, as done previously 5,26,69 . Under standard model settings 5 PIN efflux rates are equal across all cell types and hence PIN types.…”

Section: Methodsmentioning

confidence: 99%

Transport properties of canonical PIN-FORMED proteins and the role of the loop domain in auxin transport

Janacek,

Kolb,

Schulz

et al. 2024

Preprint

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Indole-3-acetic acid (IAA), the most abundant endogenous auxin is transported in plants in a polar fashion by PIN-FORMED (PIN) transporters and controls virtually all plant growth and developmental processes. Canonical PINs possess a long and largely disordered cytosolic loop domain which is shorter in non-canonical PINs. Auxin transport by canonical PINs is activated loop phosphorylation by kinases. While the structure of the transmembrane domains of these transporters was recently solved, their transport properties remained poorly characterized and particularly the relative roles of the transmembrane and loop domain therein. In this study we used flux studies to obtain quantitative kinetic parameters of IAA transport mediated by canonical PINs as well as of chimeras between transmembrane and loop domains of different PINs upon their activation by D6 PROTEIN KINASE or PINOID. We found that the transporters possess distinct transport properties that are due to both the transmembrane and loop domain. To demonstrate the physiological relevance of these distinct transport properties, we modelled root tip IAA distribution patterns and investigated the potential of different PINs to complement the agravitropic root growth phenotype of the pin2 mutant when expressed in the PIN2 domain. We found a strong correlation between transport parameters and physiological output indicating that in addition to PIN polarity a low transport rate in the PIN2 expression domain is required for gravitropic growth. Overall, the data show that the loop domain is not only required for activation of PIN-mediated auxin transport but has an additional role in the transport cycle by a currently unknown mechanism.

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Complementary roles for auxin and auxin signalling revealed by reverse engineering lateral root stable prebranch site formation

Cited by 9 publications

References 58 publications

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

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

GH3‐mediated auxin inactivation attenuates multiple stages of lateral root development

Transport properties of canonical PIN-FORMED proteins and the role of the loop domain in auxin transport

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