Cell Science at a Glance 1199

Auxin signaling Thimann, 1937). Subsequent efforts have 2003; Benková et al., 2003). Cellular
illuminated numerous physiological auxin levels results from complex
Tomasz Paciorek and Jiřˇí Friml* effects of auxin. There are many interplay between auxin synthesis,
Center for Plant Molecular Biology, University of developmental processes in which auxin degradation and (de)conjugation to/from
Tuebingen, 72076 Tuebingen, Germany plays a role, including embryo and fruit sugars and amino acids (Ljung et al.,
*Author for correspondence development, organogenesis, vascular 2005). The details of auxin biosynthesis
(e-mail: jiri.friml@zmbp.uni-tuebingen.de)
tissue differentiation, root patterning, and its regulation remain largely elusive,
Journal of Cell Science 119, 1199-1202 elongation and tropistic growth, apical but it is known that both tryptophan and
Published by The Company of Biologists 2006
doi:10.1242/jcs.02910
hook formation and apical dominance indole can serve as precursors (Cohen et
(for a review, see Kepinski and Leyser, al., 2003). The major determinant of
2005a). Some very rapid cellular asymmetric auxin accumulation is
Charles Darwin, studying the response of responses, such as plasma membrane directional, intercellular auxin transport
canary grass coleoptiles to unilateral depolarization and apoplast acidification, (Friml et al., 2002b; Weijers et al.,
light, first demonstrated the existence of have also been connected to auxin (Rück 2005). The molecular components
a moving signal that mediated plant et al., 1993; Hager, 2003). involved are the PIN and AUX1 auxin-
phototropism (Darwin, 1880). This efflux and -influx transporters,
discovery of the first plant hormone, later Asymmetric accumulation of auxin in respectively (Gälweiler et al., 1998;
termed auxin (from the Greek ‘auxein’, specific cells (sometimes called auxin Luschnig et al., 1998; Bennett et al.,
which means to grow), was followed gradients) is a necessary prerequisite for 1996). PIN proteins are thought to be
several decades later by the identification various developmental roles of auxin part of a multicomponent complex, and
of auxin as indole-3-acetic acid (IAA) (Sabatini et al., 1999; Friml et al., their polar, subcellular localisation
(Koegl and Kostermans, 1934; Went and 2002a; Friml et al., 2002b; Friml et al., determines the direction of auxin flow
Journal of Cell Science

Auxin Signaling
Tomasz Paciorek and Jiří Friml

IAAH IAA– + H+

Cell wall pH = 5.5 Plasma membrane

Cytoplasm pH = 7.0 AUX1
ER
Nucleus
I

Ub
Ub I
Ub I
I
ABP1 IAAH Ub
Ub
Ub
I
II V

AXR1 Ub

ECR1 RUB1 jcs.biologists.org

? CSN
1
2
3
7 8 4 Proteasome
GDP GNOM 6 5 RCE1
GNOM
ARF
+
IAA + H Gene expression
GTP CH 2COOH TIR
GDP SCF DBD MR
ARF
Endosome Ub III IV
CUL1 RBX1 Ub III IV or III IV
Inactive GDP N
Ub DBD MR DBD MR
I ASK1 AuxRE AuxRE
? H

TIR1
Ub
Ub

Pi I II III IV
ARF
GTP
BIG DBD MR III IV ARF
Active E2 AUX/IAA
COOH Ub I II III IV
PIN1 I
Ub II
I ? III IV
NH2 E1 I II III IV
N II III IV DBD MR
N III IV
I
H Indole H AuxRE
Tryptophan
? No gene expression
IAA IAA
? ATP ADP

?
PIN1 PGP1/PGP19 IAAH ABP1 Cell elongation

© Journal of Cell Science 2006 (119, pp. 1199-1202)

(See poster insert)

substrates. Forward genetic screens identified a RUB1-Cul1 complexes result in an AUX/IAAs have an architecture similar to group of Arabidopsis mutants able to auxin-insensitive phenotype (Leyser et that of ARFs. where the type E3 ligases is the F-box protein. 1998).. genetic evidence for the involvement of Cul1 by RUB1 seems to be very 1999). 1996). auxin rapidly (in some cases downstream signaling components has Proteasome-mediated degradation is within 3 minutes) regulates gene used virtually all possible experimental common to many fundamental cellular expression (Theologis et al. members) of transcription factors the endoplasmic reticulum. A subunit of SCF. they may mark proteins for proteasome-mediated 2001). Ulmasov et al. 1997).. This three-step part contains the conserved domains III (Steffens et al. the other interaction ABP1 in auxin-dependent development important for SCFTIR1 activity and partners of ARFs are small. which is mediated by responsive genes. mutant was isolated in a similar screen seedling lethality. 1999). 2003. Domains III and IV (related to inhibitory auxin levels [auxin-resistant Cul1 also contributes to SCFTIR1 domains III and IV of ARFs) play an (axr) mutants].. First. 1998). Much of ABP1 is localized in (Voges et al. which can signalosome (CSN) (Lyapina et al. 1993). 1992).. Thus. Mutations in the AXR1 (29 members). 2002). The molecular regulation.. 1993). TIR1 decreased degradation of SCFTIR1 substitution in this domain results in a encodes a member of large family of F. together with other components seem to signaling for plant development has 2001). encoded by the Arabidopsis genome pH is too high for efficient auxin binding which confers specificity by binding to (Ulmasov et al. 1997). provided a functional connection RUB1 (a protein related to ubiquitin and a middle region determines whether a between extracellularly localized ABP1 known as NEDD8 in mammals) to the particular ARF acts as a transcriptional and some auxin-dependent cellular cullin (Cul1) subunit of SCF (del Pozo activator or repressor. This is mediated by a important role in homodimerization and characterization of the axr1 mutant multiprotein enzymatic complex present heterodimerization with other AUX/IAAs revealed that AXR1 function is related in most eukaryotic organisms: the COP9 and ARFs.. 2006). All members of (Henderson et al. Forward genetics has thus firmly form an auxin transport network that been highlighted by the analysis of established ubiquitin-dependent protein mediates local auxin distribution and quadruple tir1-related mutants.. with the sequence TGTCTC was (ABP1) has repeatedly been identified in Then. This auxin-response factor (ARF) Journal of Cell Science role of ABP1 remains unclear (Napier et proteasome and subsequently degraded is part of a large family (with 23 al. box proteins involved in regulated mutants and are auxin resistant. isolation of the transcription factor that (Palme et al.g. Since the process again requires the coordinated and IV... 2001). in embryo development (Dharmasiri et al. importantly. 2005). Although the function of to the ubiquitylation pathway. PIN proteins importance of TIR-based auxin auxin signaling (Schwechheimer et al. homo. Deconjugation of RUB1 from domains.. The activity of the TIR1-containing architecture: the N-terminal end consists ABP1 antibodies and peptides. one of them is AXR1. approaches. short-lived is hard to obtain. Besides its strong protein ligase (E3). Interestingly.. which were identified in a screen for transcriptional repressors that allows them Further strong support for this components of the light signaling to bind DNA directly (Morgan et al. 1200 Journal of Cell Science 119 (7) (Wiśniewska et al. CSN has eight subunits. 1997b). Robinson and Ardley. the AUX/IAA. The first cohesive data processes in animals and plants (Gray Subsequent analyses revealed that many emerged from straightforward and Estelle. Such plants resemble axr1 gain-of-function mutation that stabilizes . have regulated by covalent conjugation of which interacts directly with the AuxRE. to auxin with high affinity. Domain II seems to be of particular for mutants resistant to auxin transport function mutation in subunit 5 leads to importance. including maize the target protein.. which allowed the (Hertel et al. et al. ubiquitin (Ub) is activated SAUR and GH3 families) are primary isolating proteins that specifically bind by binding to a ubiquitin-activating auxin-responsive genes (Guilfoyle.. 1999).. biochemical approaches aimed at 2004). which can specifically gene. PGP1 and PGP19 P-glycoprotein proteasome-mediated protein demonstrating the importance of the transporters are involved in auxin efflux degradation (Ruegger et al.... and the C-terminal responses. 2001).. 2000. in different The hunt for an auxin receptor and plant species. 1985). 1972) and Arabidopsis E2 in association with a ubiquitin.. this family share a very similar protein using agonistic and antagonistic anti. which serve as a platform for Arabidopsis abp1 loss-of-function action of several enzymes. especially cell expansion and Estelle.. AUX/IAA dimers is not clear. but a leaky loss-of. Modification of ARFs (Tiwari et al. as well SCF-like complex (SCFTIR1) is of a large DNA-binding domain (DBD).. ability to bind auxin. as conditional ABP1 expression. most of have a topology similar to prokaryotic degradation (Leyser et al. of the target genes (e. A single amino-acid inhibitors (Ruegger et al. In addition. 1999). The RUB1 deconjugation process for proper (Geisler et al. it is transferred onto An auxin-response element (AuxRE) protein termed auxin-binding protein 1 a ubiquitin-conjugating enzyme (E2). They consist of four elongate roots despite the presence of al. the significance normal auxin responsiveness (del Pozo nuclear proteins of the AUX/IAA family of its binding to auxin remains unclear. Experiments the substrates (Ruegger et al... It was initially shown that. 1999). that decrease the number of inhibit ARFs (Ulmasov et al. Next. connection was obtained when the pathway (Chamovitz at al. ubiquitin is covalently attached to identified in promoters of many auxin- different plant species. 1998). AUX/IAA proteins thus might also transport inhibitor response 1 (tir1) Knocking out any of these leads to directly regulate gene transcription.. The modified binds to this sequence (Ulmasov et al.. 1998).. the physiological protein is then targeted to the 26S 1997a). which degradation as an important part of triggers different cellular responses in can display dramatic patterning defects auxin signaling.and hetero-dimerization with other mutant is lethal (Chen et al. 2005b). A single enzyme (E1). various developmental contexts.

J. 1760- many details of this mechanism that remains unknown. S. 2001). N.. Sci.. 2001. Walker. Bennett. 9. J. transport components PIN1. J. pathway and promote the TIR1. R. vesicle. mediate part of the effect of auxin on membrane hyperpolarisation (Rück et al. A plausible candidate for 2002). 948-950. Callis. 15342- functional auxin receptors that mediate dependent synaptic transmission at the 15347. 1418-1422. 2001). Dev. C. (1880). but it is likely to be 1763. 109-119... J. The F-box protein TIR1 is an auxin receptor.. Sussman. S. (1998). 441-445.. the membrane and this. E. expression. C. M. P. Science 273. J.. BIG. Wisniewska. and their auxin transport inhibitors on PIN (2005a). D. Yamada. a novel multisubunits nuclear regulator involved in light control of a plant development switch. Green. M. 2005a. it ubiquitylation pathway – for example... Thus. Teichmann. 1992. as the nuclear pathway (Dharmasiri et al. 1999). Hager. del Pozo.. G. The molecular function of BIG Estelle.. efflux-dependent auxin gradients as a common al. such as how ARF is involved in some more general aspect of Dharmasiri. TIR1 functional callosin-like protein. 2005b). which means that they are very rapidly of the endocytic cycling of plasma degraded (Gray et al. T.. USA 96. occur very fast. Hobbie. M. M. Mizoguchi et and does not appear to be connected to of AUX/IAA proteins is their very short al. Cell 115. Schulz. D.. physiological roles of different big mutations also modulate the effect of Dharmasiri... 2002). clear whether there are parallel arms or of endocytosis and some other E. such whose orthologue in Drosophila is also del Pozo. M... A characteristic feature Jeromin.. 591-602. Genes Dev. Two genetically discrete pathways convert interaction of TIR1 with the AUX/IAAs auxin transport by auxin itself. Millner. many plasma membrane signal from its interaction with a function interferes with AUX/IAA proteins constantly recycle in vesicles receptor to gene expression. directly and this is sufficient to promote mechanism for a feedback regulation of Cohen. (2003). M. such as auxin module for plant organ formation. Marchant... which at the end to stabilization of AUX/IAA proteins... T. 1999) interferes understanding of the action of auxin. Sauer. S. A. MAP kinase required for rapid auxin-dependent (Worley et al. A. Trends Plant Sci.. H. half-life.. M. 2001).. J. Tian et al. (2003). 2005). M. S. C. 2001) Tian et al. Auxin instead inhibits the a permease-like regulator of root gravitropism. facilitates Chen.. J. The inhibition Dharmasiri.. and Feldmann. M. interactions with each other. These exciting results largely recycling proteins. There are still 2001). 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