ROP GTPase-Dependent Actin Microfilaments Promote PIN1 Polarization by Localized Inhibition of Clathrin-Dependent Endocytosis

Nagawa, Shingo; Xu, Tongda; Lin, Deshu; Dhonukshe, Pankaj; Zhang, Xingxing; Friml, Jiřı́; Scheres, Ben; Fu, Ying; Yang, Zhenbiao

doi:10.1371/journal.pbio.1001299

Cited by 183 publications

(193 citation statements)

References 63 publications

(110 reference statements)

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“…2002). ABP1 is involved in: regulation of the membrane potential and ion fluxes; elevation in cytosolic Ca 2+ concentration (Shishova and Lindberg 2010) and changes in the cytoskeleton (Nagawa et al 2012), in the vesicular trafficking (Robert et al 2010), in the cell division and expansion (Braun et al 2008).…”

Section: Discussionmentioning

confidence: 99%

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

2017

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Section: Discussionmentioning

confidence: 99%

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

2017

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“…Mutations impairing starch biosynthesis, biogenesis, and sedimentation of starch-containing plastids (i.e., statoliths) and their interactions with actin filaments, endoplasmic reticulum, and plasma membrane highlight the importance of mechanosensitive ion channels and components of calcium/calmodulin and inositol-phosphate signaling pathways that connect gravisensing with the regulation of polar localization of PINs and PGPs (Baldwin et al, 2013;Blancaflor, 2013;Kurusu et al, 2013). Emerging data indicate that cortical actin accumulation regulates clathrin-dependent endocytosis Nagawa et al, 2012), whereas enhanced inositol triphosphate and Ca 2+ levels decelerate exocytosis of PIN1 and PIN2 similarly to mutations of inositol polyphosphate 1-phosphatase and phosphatidylinositol monophosphate 5-kinase genes (Zhang et al, 2011;Mei et al, 2012). Furthermore, signaling through the 3-phosphoinositidedependent kinase1 and interactions with Ca 2+ binding or calmodulinlike proteins appear to regulate the activity of AGC kinases that phosphorylate central hydrophilic loops of PINs, as well as ABCB/ PGPs (Benjamins et al, 2003;Zegzouti et al, 2006;Henrichs et al, 2012;Rademacher and Offringa, 2012).…”

Section: Introductionmentioning

confidence: 99%

Inactivation of Plasma Membrane–Localized CDPK-RELATED KINASE5 Decelerates PIN2 Exocytosis and Root Gravitropic Response inArabidopsis

et al. 2013

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CRK5 is a member of the Arabidopsis thaliana Ca 2+ /calmodulin-dependent kinase-related kinase family. Here, we show that inactivation of CRK5 inhibits primary root elongation and delays gravitropic bending of shoots and roots. Reduced activity of the auxin-induced DR5-green fluorescent protein reporter suggests that auxin is depleted from crk5 root tips. However, no tip collapse is observed and the transcription of genes for auxin biosynthesis, AUXIN TRANSPORTER/AUXIN TRANSPORTER-LIKE PROTEIN (AUX/LAX) auxin influx, and PIN-FORMED (PIN) efflux carriers is unaffected by the crk5 mutation. Whereas AUX1, PIN1, PIN3, PIN4, and PIN7 display normal localization, PIN2 is depleted from apical membranes of epidermal cells and shows basal to apical relocalization in the cortex of the crk5 root transition zone. This, together with an increase in the number of crk5 lateral root primordia, suggests facilitated auxin efflux through the cortex toward the elongation zone. CRK5 is a plasma membrane-associated kinase that forms U-shaped patterns facing outer lateral walls of epidermis and cortex cells. Brefeldin inhibition of exocytosis stimulates CRK5 internalization into brefeldin bodies. CRK5 phosphorylates the hydrophilic loop of PIN2 in vitro, and PIN2 shows accelerated accumulation in brefeldin bodies in the crk5 mutant. Delayed gravitropic response of the crk5 mutant thus likely reflects defective phosphorylation of PIN2 and deceleration of its brefeldin-sensitive membrane recycling.

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“…Even more interestingly, this data is opposite to the one resulting from ABP1 inactivation (Fig. 3), whereas both endocytosis inhibitors and ABP1 inactivation impair endocytosis clathrin-dependent 13,32 . It clearly indicates that in no way at all the enhanced degradation of AUX/IAA after functional inactivation of ABP1 is originated from endocytosis inhibition.…”

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confidence: 64%

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

et al. 2013

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Auxin is a major plant hormone that controls most aspects of plant growth and development. Auxin is perceived by two distinct classes of receptors: transport inhibitor response 1 (TIR1, or auxin-related F-box (AFB)) and auxin/indole-3-acetic acid (AUX/IAA) coreceptors, that control transcriptional responses to auxin, and the auxin-binding protein 1 (ABP1), that controls a wide variety of growth and developmental processes. To date, the mode of action of ABP1 is still poorly understood and its functional interaction with TIR1/AFB-AUX/IAA coreceptors remains elusive. Here we combine genetic and biochemical approaches to gain insight into the integration of these two pathways. We find that ABP1 is genetically upstream of TIR1/AFBs; ABP1 knockdown leads to an enhanced degradation of AUX/IAA repressors, independently of its effects on endocytosis, through the SCF TIR1/AFB E3 ubiquitin ligase pathway. Combining positive and negative regulation of SCF ubiquitin-dependent pathways might be a common mechanism conferring tight control of hormone-mediated responses.

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ROP GTPase-Dependent Actin Microfilaments Promote PIN1 Polarization by Localized Inhibition of Clathrin-Dependent Endocytosis

Abstract: A study in leaf epidermal pavement cells reveals that auxin activation of a Rho-like GTPase from plants induces inhibition of endocytosis through the clathrin-mediated pathway by regulating the accumulation of cortical F-actin.

Cited by 183 publications

References 63 publications

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

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

Inactivation of Plasma Membrane–Localized CDPK-RELATED KINASE5 Decelerates PIN2 Exocytosis and Root Gravitropic Response inArabidopsis

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

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