Cell Surface- and Rho GTPase-Based Auxin Signaling Controls Cellular Interdigitation in Arabidopsis

Abstract

Summary Auxin is a multi-functional hormone essential for plant development and pattern formation. A nuclear auxin signaling system controlling auxin-induced gene expression is well established, but cytoplasmic auxin signaling as in its coordination of cell polarization is unexplored. We found a cytoplasmic auxin signaling mechanism that modulates the interdigitated growth of Arabidopsis leaf epidermal pavement cells (PCs), which develop interdigitated lobes and indentations to form a puzzle-piece shape in a two-dimensional plane. PC interdigitation is compromised in leaves deficient in either auxin biosynthesis or its export mediated by PINFORMED 1 localized at the lobe tip. Auxin coordinately activates two Rho GTPases, ROP2 and ROP6, which promote the formation of complementary lobes and indentations, respectively. Activation of these ROPs by auxin occurs within 30 seconds and depends on AUXIN-BINDING PROTEIN 1. These findings reveal Rho GTPase-based novel auxin signaling mechanisms, which modulate the spatial coordination of cell expansion across a field of cells.

A comparison of the effects of 1,4-naphthoquinone and 2-hydroxy-1,4-naphthoquinone (lawsone) on indole-3-acetic acid (IAA)-induced growth of maize coleoptile cells

“…Taking above into account it can be suggested that 1,4naphthoquinone and 2-hydroxy-1,4-naphthoquinone can similarly affect auxin nuclear signaling system. Furthermore, it can be suggested that naphthoquinones can interfere the cytoplasmic auxin signaling mechanisms consisting of ABP1 (auxin binding protein 1), TMK (transmembrane kinase) and ROPs (Rho-like GTPase) (Xu et al 2010(Xu et al , 2014Grones et al 2015). ABP1 is membrane auxin receptor and is crucial for mediating a range of auxin fast non-transcriptional effects.…”

Auxin-Binding Protein 1 is a negative regulator of the SCFTIR1/AFB pathway

“…We showed that modification of endocytosis is not essential for the control of AUX/IAA homeostasis by the ABP1-dependent pathway, thus splitting ABP1 effects into two diverging pathways. Determining whether ROP/RAC GTPases, which were shown to act on endocytosis 11,12 , are also part of the ABP1 pathway controlling AUX/IAA stability and gene regulation will be an important question. Interestingly, tobacco and Arabidopsis RAC GTPases were reported to mediate auxin-responsive gene expression 40 and to induce formation of proteolytically active nuclear protein bodies containing AUX/IAA proteins 33 .…”

“…Loss of function of up to four TIR1/AFB proteins leads to three different phenotypes ranging from rootless seedlings (group I) to nearly normal ones (group III) 9 . In addition to TIR1/AFB-AUX/IAA coreceptors, auxin is also perceived by ABP1 that is associated with the plasma membrane and was shown to be involved in the regulation of ion fluxes at the plasma membrane 10 and, more recently, in the activation of ROP GTPases 11,12 in response to auxin. ABP1 was also shown to be essential for clathrindependent endocytosis, acting as a positive factor for clathrin recruitment to the plasma membrane and inhibiting this process after binding to auxin 11,13 .…”

In vivomonitoring of plant small GTPase activation using a Förster resonance energy transfer biosensor

“…The subsequent immunoblotting assay can quantify Rac/ROP activation in cells by determining the amount of activated Rac/ROP. This is a widely used method for the semi-quantitative measurement of Rac/ROP activity from plants to animals (17,18,20). However, the PAK CRIB pull-down assay only provides a snapshot, and cannot detect the spatial and temporal dynamics of intracellular signaling in living cells.…”