Regulation of auxin transport polarity by AGC kinases

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Regulation of auxin transport polarity by AGC kinasesHelene S Robert1 and Remko Offringa

The plant hormone auxin controls plant development

through gradients and maxima that are generated by PIN

efflux carrier driven polar auxin transport. PIN proteins direct

this cell-to-cell auxin transport, and thus orient plant

development through their asymmetric subcellular distribution.

PIN polarity is regulated by PINOID and the phototropins,

members of the AGC protein serine/threonine kinase family.

Here we review the signaling pathways of these kinases and the

role of calcium and BTB proteins in translating both internal and

external signals into developmental responses via PIN

relocalization, to adapt plant development to changing

environmental conditions.

Addresses

Department of Molecular and Developmental Genetics, Institute of

Biology, Leiden University, Wassenaarseweg 64, 2333 AL Leiden, The

Netherlands

Corresponding author: Offringa, Remko

([email protected])1Current address: Department of Plant Systems Biology, VIB, Ghent

University, Technologiepark 927, 9052 Ghent, Belgium.

Current Opinion in Plant Biology 2008, 11:1–8

This review comes from a themed issue on

Cell Signalling and Gene Regulation

Edited by Jason Reed and Bonnie Bartel

1369-5266/$ – see front matter

# 2008 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2008.06.004

IntroductionAs sessile organisms, plants have developed various

mechanisms for perceiving and responding to changes

in environmental conditions, such as light, temperature,

and drought. Studies of Darwin on the tropic bending of

canary grass and oat coleoptiles toward a unidirectional

light source provided the first indications of a transported

growth substance that mediates this adaptive response. A

few decades later, the Dutch botanist Went was the first

to isolate this growth substance, which was identified as

the signaling molecule indole-3-acetic acid (IAA) and

named auxin after the Greek word for ‘to grow’. The

asymmetric lateral distribution of auxin during tropic

responses was found to be mediated by its polar cell-

to-cell transport. This polar auxin transport (PAT) is

crucial for many developmental processes, creating auxin

gradients and maxima that regulate cell division,

elongation, and differentiation, and in this way are instru-

Please cite this article in press as: Robert HS, Offringa R, Regulation of auxin transport polarit

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mental for plant architecture and for its adaptation to

environmental changes [1].

The drivers of the auxin transport pathwayMolecular genetic research in Arabidopsis has identified

PIN-FORMED (PIN) transmembrane proteins as auxin

efflux carriers that determine the direction of PAT

through their asymmetric subcellular localization

[1,2�,3�]. The Arabidopsis thaliana genome has eight

PIN genes. The function of five of the encoded proteins

has been analyzed in detail, whereas that of PIN5, PIN6,

and PIN8 remains to be uncovered [1]. Besides PIN

proteins, the P-glycoprotein (PGP)-type ABC (ATP-

binding cassette) transporters, PGP1, and PGP19, have

been shown to act as auxin efflux carriers [2�,4]. Arabi-

dopsis PGP1 and PGP19 co-localize with PIN1 and PIN2

in root and shoot cells and enhance auxin transport

activity by physically interacting with these PINs [5].

Their predominantly apolar subcellular localization

suggests that PGPs are not major determinants in the

directionality of PAT [5]. PGP-type ABC transporters are

found from unicellular algae to angiosperms, and are

likely to be the ancient auxin efflux carriers, whereas

polar PIN proteins occur only later in evolution in multi-

cellular land plants for which directional auxin transport

has become a crucial aspect of development [6��]. In

addition to auxin efflux carriers, the AUXIN RESIST-

ANT1 (AUX1) permease-like protein and three homolo-

gous Like-AUX1 (LAX) proteins were identified in

Arabidopsis as auxin influx carriers [7,8]. AUX/LAX are

important enhancers of auxin transport and seem to

contribute to the directionality of PAT through feedback

on PIN polarity [9]. As PIN proteins are clearly the crucial

drivers of PAT, we will focus this review on the signaling

pathways that determine their asymmetric subcellular

localization and thereby modulate developmental pro-

grams in response to environmental stimuli.

General mechanisms in PIN polarity dynamicsPIN polar localization is highly dynamic, is regulated by

vesicle trafficking, protein degradation, and phosphoryl-

ation, and is responsive to both external and internal

signals, among which auxin [10–14]. Cyclic trafficking

of PIN-loaded vesicles was first demonstrated by using

the fungal antibiotic Brefeldin A (BFA) [10]. BFA blocks

exocytosis by targeting the large guanine nucleotide

exchange factors for the ARF-type G proteins (ARF-

GEFs) involved in endosomal recycling (Figure 1). In

Arabidopsis root cells, PIN1 basal polar recycling requires

the BFA-sensitive ARF-GEF GNOM, while apical recy-

cling of PIN2 and AUX1 is mediated by BFA-resistant

ARF-GEFs [10,11��,15]. Moreover, the basal retargeting

y by AGC kinases, Curr Opin Plant Biol (2008), doi:10.1016/j.pbi.2008.06.004


http://dx.doi.org/10.1016/j.pbi.2008.06.004

mailto:[email protected]


2 Cell Signalling and Gene Regulation


Figure 1

Model for the role of the PINOID (PID) kinase as key regulator of the dynamic polar subcellular localization of PIN auxin efflux carriers. PIN proteins are

polarly localized auxin efflux carriers [1]. For a rapid regulation of their localization, they cycle between endosomal membrane compartments and the

plasma membrane, via exocytosis and clathrin- and sterol-dependent endocytosis [10,16,18]. This trafficking requires the action of ARF-GEF proteins.

In the basal PIN cycling pathway, the BFA-sensitive ARF-GEF GNOM is involved in exocytosis [10], whereas the BFA-resistant GNOM-LIKE1 (GNL1) is

thought to be required for endocytosis [17]. Other BFA-resistant ARF-GEF proteins are likely to be involved in the apical cycling route of PIN-loaded

vesicles. Movement of PIN-cargoes between the basal and apical cycling pathways is occurring via transcytosis [11��]. The PINOID (PID) protein

serine/threonine kinase is a membrane-associated protein that labels PIN cargoes for trafficking to the apical plasma membrane by phosphorylating

the hydrophilic loop of PIN proteins [22��]. Whether PID acts at the apical or basal plasma membrane or in endosomal compartments is not yet known.

PID activity is negatively or positively regulated through its calcium-dependent interaction with the calcium-binding proteins TOUCH3 (TCH3) or

PINOID-BINDING PROTEIN1 (PBP1), respectively [32]. Elevated auxin concentrations are well known to increase cytosolic calcium [27–30] and, apart

from the positive effect of auxin on PID expression [21], this could provide a second feedback loop by which auxin directs its own transport by

regulating the subcellular localization of PIN proteins.

of PIN1 during embryogenesis and lateral root formation

involves ARF-GEF-dependent transcytosis (Figure 1)

[11��]. This trafficking of PIN-loaded vesicles is actin

dependent [10] and PIN endocytosis is clathrin depend-



ent [16] and thought to be mediated by the BFA-resistant

GNOM-like 1 (GNL1) [17]. The membrane sterol com-

position is an important factor for polar endocytic recy-

cling of membrane proteins, and the polar localization of




Kinases orienting auxin transport Robert and Offringa 3


PIN1, PIN2, PIN3, and AUX1 is altered by mutations or

drug treatments affecting sterol composition [15,18,19].

In addition to protein targeting as a control for the

direction of PAT, protein degradation and turnover were

shown to feedback on the plasma membrane localized

PIN protein abundance in response to environmental

cues such as light and gravity. PIN2 is ubiquitinated

and degraded at the upper side of the root upon gravi-

stimulation [12] and in dark grown roots several PINs and

AUX1 are targeted to the vacuole for degradation [20].

AGC kinases as regulators of auxin transportpolarityThe first, and yet only identified molecular determinant

in the polar distribution of PINs is the PINOID (PID)

serine/threonine protein kinase [13]. Above threshold

levels of PID activity were found to induce movement

of PIN proteins from the basal (root tip facing) to the

apical (shoot tip facing) side of Arabidopsis root cells,

whereas in embryos and inflorescence tip epidermis cells,

loss-of-function pid mutations cause an apical-to-basal

shift [13]. In both cases, alteration of PIN polarity changes

the direction of PAT (Figure 1) and explains the pheno-

types of PID loss- and gain-of-function mutants. These

results indicate that PID-dependent phosphorylation is

instructing for PIN apical localization. Interestingly, PIDis an auxin responsive gene [21], suggesting that PID is

part of a feedback loop by which auxin controls the

direction of its own transport [14]. Recently it has been

demonstrated that PID directly phosphorylates PIN

proteins in their large central hydrophilic loop

(Figure 1) and that PP2A phosphatases counteract the

activity of this kinase [22��]. The kinase and the phos-


Figure 2

Developmental processes involving AGC kinase dependent PIN relocalizatio

PIN1::PIN1:GFP expression (light blue, plasma membrane) marks the incipie

nuclear) reported auxin maxima that persist in more mature primordia (P1–P

dark-grown wild-type Arabidopis (b) or phot1 mutant (C) seedlings following

Galvan-Ampudia); (d and e), Gravitropic growth of wild-type Arabidopsis se

hook-like structure at the root tip of 35S:PID seedlings, indicative for root m


phatases co-localize with PINs at the plasma membrane,

and probably also in intracellular compartments [22��].Similar to PID overexpression (Figure 2e), loss of PP2Afunction results in root agravitropism and root meristem

collapse, which can be partially rescued by pid loss-of-

function. In correlation with these seedling phenotypes,

PIN localization in pp2a mutants is apical in Arabidopsis

roots. Although these data show that direct phosphoryl-

ation is an important signal in PIN polar targeting [22��],the actual mechanism behind the PIN polarity establish-

ment is still unclear. Key questions to address are (1)

where in the cell does PID dependent PIN phosphoryl-

ation occur, (2) how does the phosphorylation status of the

PINs signal their incorporation in the basal (GNOM

dependent and GNL1 dependent) or apical cycling route,

(3) are other PID phosphorylation targets involved or is

PIN phosphorylation sufficient, and (4) if PID-dependent

phosphorylation determines apical PIN localization, what

signals instruct lateral or basal PIN localization?

An answer to this last research question may come from

studying the PID-like kinases. PID belongs to the AGC

family of serine/threonine kinases, which includes and is

named after the well studied animal kinases (PKA, –G

and –C) that are involved in receptor mediated growth

factor signal transduction. In plants, the typical PKA,

PKG, and PKC are not present, but instead the plant-

specific subfamily of the AGC kinases, AGCVIII, has

been identified [6��]. In Arabidopsis, this family com-

prises PID, which groups to the AGC3 clade together

with WAG1 and WAG2, and the phototropins PHOT1

and PHOT2, blue light receptors that trigger phototropic

growth [6��,23]. Functional analysis of WAG1 and WAG2


n. (a) Phyllotactic patterning in the inflorescence apex [44]. Elevated

nt primordium I1 and precedes the DR5rev::3xVENUS-N7 (orange,

4, image kindly provided by Marcus Heisler); (b and c), A four-day-old

4 h stimulation with unidirectional light (images kindly provided by Carlos

edlings (d) and agravitropic growth of 35S::PID seedlings (e). Note the

eristem collapse [21].





indicated that these kinases play a role in root growth.

The enhanced sensitivity of root growth of wag1 wag2loss-of-function seedlings to the PAT inhibitor NPA [23],

and the fact that the WAG kinases, like PID, are plasma

membrane-associated together suggest that the WAG

kinases are also involved in the regulation of PIN polar

targeting [6��].

Regulators of the PAT regulatorsPDK1

A common feature of animal AGC kinases is their acti-

vation by the 3-phosphoinositide dependent protein

kinase1 (PDK1). In animal cells, PDK1 recruits the kinases

by binding to their hydrophobic C-terminal PDK1 Inter-

acting Fragment (PIF) domain, and activates or enhances

the activity of the kinase by phosphorylation [24]. The

majority of the Arabidopsis AGCVIII kinases, including

PID, but excluding WAG1, WAG2, PHOT1, or PHOT2,

have a PIF domain and are in vitro substrates of PDK1

[25,26]. However, the in planta significance of their PDK1-

dependent phosphorylation is still unclear. PID, for

example, is an auto-activating kinase, and it may therefore

not need PDK1 during standard developmental programs,

but only to induce changes in PIN polarity in response to

specific stress conditions such as wounding [14].

Calcium signaling

Calcium has been reported as modulator of auxin responses

and PAT. A rapid increase in the cytosolic calcium con-

centration was detected within minutes after auxin appli-

cation using calcium fluorescent dyes or ion-sensitive

electrodes [27–29]. It was also found that PAT is sup-

pressed by application of the calcium chelator EDTA and

restored after application of a calcium solution [30]. Inter-

estingly, the PID kinase interacts with two calcium-bind-

ing proteins, TOUCH3 (TCH3) and PINOID BINDING

PROTEIN1 (PBP1), in a calcium-dependent manner, a

finding that provided the first molecular link between

calcium signaling and PAT [31]. TCH3 is a calmodulin-

like protein with six EF-hand domains encoded by a touch-

responsive gene [32]. PBP1 is a small protein with a single

EF-hand [33]. On the basis of in vitro phosphorylation

assays, neither of the calcium binding proteins is phospho-

target of PID, and instead, TCH3 represses, whereas PBP1

enhances PID kinase activity [31]. Recent results indicate

that this calcium-dependent regulation by TCH3 and

PBP1 is conserved for all four AGC3 kinases [Robert,

Galvan-Ampudia, and Offringa, unpublished].

For speculations on the in vivo significance of calcium in

regulating the AGC3 kinases, a first hint comes from the

phototropin signaling pathway. Phototropins consist of a

C-terminal kinase domain and an N-terminal photo-

receptor domain containing two LOV domains that bind

the chromophore flavin mononucleotide [34]. In dark,

PHOT is membrane-associated with both LOV domains

repressing the activity of the kinase domain. Light stimu-



lation results in the release of the LOV-dependent repres-

sion on the kinase domain [34], and an early event in the

transduction cascade is PHOT dependent calcium

release from the apoplast through plasma membrane

channels [35]. Although the role of calcium in the photo-

tropic response remains to be elucidated, an interesting

possibility could be that PHOT signaling initiates relo-

calization of PINs, by modulating the activity of the

AGC3 kinases through their calcium-induced interaction

with TCH3 and PBP1 (Figure 1).

BTB proteins

Recent results suggest the involvement of Broad-Com-

plex, Tramtrack, Bric-a-Brac (BTB) scaffold proteins in

the PID signaling pathway [36�,37�]. Scaffold proteins are

characterized by the presence of multiple protein–protein

interaction domains and are important for assembling

transcription and signaling complexes. BTB domain

proteins have been first described in Drosophila melano-gaster as scaffolds in transcription complexes, are found in

many eukaryotes including mammals and plants, and are

involved in various cellular processes [38,39]. The Arabi-

dopsis genome encodes 80 BTB proteins that have been

classified in 10 subfamilies on the basis of homology and

the presence of other domains [39].

Independent mutant screens identified the BTB protein

MACCHI-BOU4/ENHANCER OF PINOID/NAKED

PINS IN YUC MUTANTS1 (MAB4/ENP/NPY1) of

the NPH3-like family as a component in the PID path-

way, either as a PID interactor, an upstream regulator of

PID transcription, a downstream phospho-target of PID,

or in a parallel signaling pathway. mab4/npy1 loss-of-

function phenotypes suggest auxin transport defects

[36�,37�], and genetic analysis of mab4 indicates that

MAB4/ENP/NPY1 is involved in organogenesis synergis-

tically with PID by controlling PIN1 localization in

embryo and inflorescence meristems [36�].

Interestingly, two other BTB domain proteins of the

NPH3-like family, NON-PHOTOTROPIC HYPOCO-

TYL3 (NPH3) and ROOT PHOTOTROPISM2

(RPT2), interact with the phototropins [40,41]. Genetic

analyses suggest that both BTB proteins are required for

the phototropic response, with nph3 resembling phot1 and

rpt2 phenocopying phot2, indicating that they are down-

stream components of the PHOT1 and the PHOT2

signaling pathways, respectively. They are both associ-

ated with the plasma membrane where they may be part

of a PHOT complex in darkness [34,40,41]. Recent data

indicate that NPH3 is phosphorylated in the dark and that

its dephosphorylation in the light is dependent on

PHOT1 [42]. The two BTB proteins are proposed to

act as modular scaffold proteins bringing together a

dynamic signaling complex comprising PHOT1, or

PHOT2, and early actors of the phototropic response

such as phosphatases and kinases [40]. The possible






interaction of NPH3 with CUL3 suggests that NPH3-

dependent recruitment of proteins for degradation by the

26S proteasome may be a crucial part of the phototropic

response [42].

Auxin dependent developmental processesregulated by plant AGC kinasesFrom the previous it becomes clear that the AGC3

kinases and phototropins are key switches that through

regulation of their expression and activity integrate many

biotic and abiotic signals to orient plant development by

directing PAT. Below we will use specific developmental

processes to exemplify how we think these kinases direct

PAT dependent patterning and growth (Table 1).

Organogenesis

Auxin plays a crucial role in the positioning and emer-

gence of new organs, such as lateral roots, leaves, and

flowers. In fact, auxin maxima precede the occurrence,

and thus indicate the positions of future organ primordia,

and the auxin efflux carrier PIN1 and the auxin influx

carrier AUX1 act in concert to generate such maxima

[1,9,43]. In the shoot apex, PIN1 is active in the epider-

mis, where its frequent polarity changes coincide with

new organ initiation (Figure 2a). Most of the current

mathematical models on the patterning of aerial organs

(phyllotaxis) assume that PIN1 polarity is self-directing to

cells with the highest auxin concentration, thereby orga-

nizing auxin maxima [44]. An important role for PID in

controlling PIN1 polarity during phyllotactic patterning is

evident, but it is not easy to envisage how the simple PID

dependent basal-to-apical switch in PIN1 polarity can

regulate this complex process [13]. Moreover, in contrast

to pin1 apices, the pin-like apex of the pid mutant does

still show phyllotactic patterning when auxin-containing

lanoline paste is applied [43]. An interesting possibility is

that the other AGC3 kinases may act partially redundant

with PID in elaborating PIN1 dynamics.


Table 1

Comparison of the developmental signaling pathways and their influ

phototropism, and gravitropism

Organogenesis

AGC kinases PINOID [13,43] PHO

Tran

Calcium ? Incre

calci

upon

Calcium BPs TCH3?, PBP1 [unpublished] ?

BTB proteins MAB4/ENP/NPY1 [36�,37�] NPH

PIN polarity changes PIN1 [13] PIN3

Direction of auxin transport Upward toward the shoot

tip [43]

Later

of th

Position of resulting

auxin maximum

At the future primordium

[43]

In th

side

Growth response Organ initiation [43] Hypo

the li


One of the earlier phyllotaxis models implied mechanical

buckling between organ primordia as a positioning mech-

anism [45]. In view of the current auxin-based models,

however, a prominent role for mechanical force in phyl-

lotaxis is questionable [44]. Still, organ formation has

been found to be responsive to touch [46], and we there-

fore speculate on the involvement of mechanical stress

increased intracellular calcium in regulating PAT by

modulating the activity of the AGC3 kinases through

their interaction with the calcium-binding proteins

TCH3 and PBP1 [31]. Together with the BTB domain

scaffold protein MAB4/ENP/NPY1 [36�,37�], they inte-

grate auxin- and mechanico-signaling to fine tune the

PAT driven phyllotactic program in response to external

signals.

Phototropism

Phototropism is the blue light phototropin receptor trig-

gered differential cellular expansion between the lit side

and the shaded side resulting in bending of a plant organ

toward or away from a unidirectional light stimulus

(Figures 2b and c) [40]. To corroborate Darwin’s initial

hypothesis, DR5 promoter–reporter gene fusions and

auxin measurements have been used to show that this

growth response in hypocotyls or coleoptiles of etiolated

seedlings is mediated by lateral movement of auxin from

the lit to the shaded side [47–50]. Arabidopsis pin3 loss-of-

function mutants are defective in phototropic responses

and PIN3 proteins show lateral localization in the hypo-

cotyl [47]. The current model involves phototropin-

induced changes in PIN3 localization, which induces

lateral auxin transport to the dark side of the hypocotyl.

One interesting possibility is that the PHOT1-induced

calcium peaks modulate the activity of PID or the other

AGC3 kinases via their interaction with TCH3 and PBP1.

On the contrary, the expression of WAG kinases is rapidly

downregulated by light [23], which might provide an

alternative or parallel mechanism of downregulating


ence on auxin distribution, and transport during organogenesis,

Phototropism Gravitropism

T1, PHOT2 [40] AGC3?

sduction: AGC3? [42]

ased cytosolic

um concentration

light stimulation [35]

Calcium transport upon

gravi-stimulus [54,55]

?

3, RPT2 [40,41] ?

[47] PIN3 [47]

al toward the shaded side

e hypocotyl [47,48]

Lateral toward the lower

side of the root tip [51,52]

e epidermis at the shaded

of the hypocotyl [47,49]

In the lateral root cap and epidermis

at the lower side of the root [51,52]

cotyl bending toward

ght source [47–49]

Root tip bending toward

the gravity vector [43,51,53]





AGC3 kinase activity and makes WAG1 and WAG2

candidate mediators of the phototropic growth responses.

As described above, the BTB protein NPH3 is a crucial

component in PHOT1 signaling. NPH3 is phosphory-

lated in the dark and dephosphorylated in a blue light

PHOT1-dependent manner [40,42,50]. Again, the AGC3

kinases may play a role in keeping NPH3 in the phos-

phorylated state that interacts with PHOT1, while repres-

sion of kinase activity followed by dephosphorylation of

NPH3 may lead to its release to the cytosol, where its

interaction with CUL3 initiates changes in PAT. NPH3

may be involved in transcriptional repression of WAG1 or

WAG2, or in mediating direct turnover of PIN3 at the lit

side.

Gravitropism

Another growth response orienting plant development is

gravitropism, the differential growth induced by changes

in the gravity vector (Figure 2d). Gravity is sensed by

plastid-derived-starch-filled organelles, which are found

in specialized cells in the columella root cap and in the

stem endodermis. Gravitropic growth of the root is well

studied, and dynamic auxin movement to the lower side

of gravi-stimulated root tips was observed using auxin

responsive DR5 promoter–reporter constructs [1,47,51].

The auxin efflux carriers PIN2 and PIN3 and the auxin

influx carrier AUX1 are the main players directing PAT

during root gravitropism. The PIN3 auxin efflux trans-

porter randomly localizes at the plasma membrane in the

root columella initials but rapidly relocates to the bottom

side of the cells upon changes in the gravity vector [47],

thereby initiating lateral movement of auxin to the lower

side of the root. PIN2 driven and AUX1 dependent

basipetal PAT via lateral root cap and the epidermis cells

subsequently establishes the auxin gradient that leads to

differential elongation between the upper and the lower

sides and results in the root reorientation toward the

gravity vector [1,51,52]. The PIN2 internalization and

degradation at the apical side [12] and its auxin-enhanced

plasma membrane localization at the basal side [12,53] act

synergistically to exaggerate this response. Curiously,

although PID overexpression induced PIN apicalization

leads to agravitropic root growth (Figure 2e); no AGC

kinase, or linked calcium binding or BTB protein has yet

been shown to be involved in root gravitropism response.

Moreover, the polarity of PIN3 does not seem to be

sensitive to PID overexpression [13]. However, in view

of the role of the WAG kinases in root waving [23] and the

role of calcium in PAT-directed gravitropism [54,55], it is

likely that the AGC3 kinases and their calcium binding

proteins play a regulatory function in gravitropic root

growth.

ConclusionsThe above indicates that specific plant AGC kinases are

key switches in the modulation of PAT to orient plant

development. The interaction of AGC3 kinases with



calcium binding proteins clarifies the observed role of

calcium signaling in the regulation of PAT. Furthermore,

BTB proteins act as scaffolds of protein complexes in the

phototropin and the PID pathways. Further research is

needed to establish the connection between environmen-

tal signals, calcium signaling, and kinase dependent PIN

polarity, and the function of BTB proteins in the AGC

kinase signaling pathways. An elegant model suggests

that the AGC3 kinases could be the plant compass that

integrates different signals to direct PAT and thereby

orients plant development [6��]. It would be of extreme

interest to validate this hypothesis and to establish if and

how phosphorylation by these kinases differentiates PIN

polar targeting. ARF-GEFs, sterols, and BTB proteins are

all potential polarity marks that could assist in sorting

cargoes to specific cycling pathways in the cell on the

basis of their phosphorylation status.

AcknowledgementsWe would like to thank Marcus Heisler and Carlos Galvan-Ampudia forproviding images for Figure 2.

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� of special interest

�� of outstanding interest

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22.��

Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A,Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F et al.:Antagonistic regulation of PIN phosphorylation by PP2A andPINOID directs auxin flux. Cell 2007, 130:1044-1056.

This work unraveled the mechanism by which the PINOID kinase isapically targeting the PIN proteins and discovered the antagonisticcomponents of PINOID in this signaling pathway. Not only the pheno-types of loss- and gain-of-function mutants in PINOID and PP2A, but alsothe activity of the two enzymes are shown to be complementary.

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These two papers describe the identification of an NPH3-like protein bymutant screens for alteration of organogenesis. NPH3 proteins are alsoinvolved in the phototropins signaling pathway, which allows to hypothe-size on an interesting parallel between the phototropism and organogen-esis signaling pathways.

37.�

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These two papers describe the identification of an NPH3-like protein bymutant screens for alteration of organogenesis. NPH3 proteins are alsoinvolved in thephototropinssignalingpathway,which allows tohypothesizeon an interesting parallel between the phototropism and organogenesissignaling pathways.

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Regulation of auxin transport polarity by AGC kinases

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