TRPLSC-1043; No.
of Pages 9
Review
ABA transport and transporters
Yann Boursiac, Sophie Léran, Claire Corratgé-Faillie, Alain Gojon,
Gabriel Krouk, and Benoı̂t Lacombe
Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes ‘Claude Grignon’,
UMR CNRS/INRA/SupAgro/UM2, Place Viala, 34060 Montpellier cedex, France
Abscisic acid (ABA) metabolism, perception, and trans-
port form a triptych allowing higher plants to use ABA as
a signaling molecule. The molecular bases of ABA me-
tabolism are now well described and, over the past few
years, several ABA receptors have been discovered. Al-
though ABA transport has long been demonstrated in
planta, the first breakthroughs in identifying plasma
membrane-localized ABA transporters came in 2010,
with the identification of two ATP-binding cassette
(ABC) proteins. More recently, two ABA transporters
in the nitrate transporter 1/peptide transporter (NRT1/
PTR) family have been identified. In this review, we
discuss the role of these different ABA transporters
and examine the scientific impact of their identification.
Given that the NRT1/PTR family is involved in the trans-
port of nitrogen (N) compounds, further work should
determine whether an interaction between ABA and N
signaling or nutrition occurs.
ABA in action
ABA is a phytohormone that was discovered during the
early 1960s, when it was found to be involved in the control
of seed dormancy and organ abscission [1–3]. Its role has
since been broadened to the regulation of development and
the adaptation of plants to adverse conditions. Because of
this, ABA is one of the most-studied hormones in applied
and fundamental plant science research [4,5].
The accepted definition of a hormone is a biological
molecule with different sites for synthesis and perception.
As a consequence, hormone action can be split into three
steps: (i) synthesis or metabolism; (ii) transport; and (iii)
perception (Figure 1). With regard to ABA, de novo syn-
thesis from carotenoids, as well as cleavage of inactive
conjugated ABA, allow pools of free ABA to increase [6].
ABA then has to be transported from the site of synthesis to
the site of action, where ABA receptors decode the mes-
sage. In this review, we discuss the journey of ABA from its
sites of synthesis to its sites of action and the need for ABA
transporters (for a full review on ABA signal transduction,
see [7–11]). Because ABA transport might occur at both
sites of synthesis and of perception, we briefly describe
both of these roles. We also present and discuss the molec-
ular cloning and functional characterization of three ABA
transporters in the context of their membership of the ABC
and PTR families.
Corresponding author: Lacombe, B. (benoit.lacombe@supagro.inra.fr).
1360-1385/$ – see front matter
ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/
j.tplants.2013.01.007
From synthesis to perception: transport steps across
membranes?
Metabolic pathways leading to free active ABA have been
elucidated. The last three steps of ABA synthesis involve:
plastidic 9-cis-epoxycarotenoid dioxygenases (NCED), cy-
tosolic short-chain dehydrogenases/reductases (SDR), such
as ABA2 in Arabidopsis (Arabidopsis thaliana), and alde-
hyde oxidases (AAO) [6,12]. These synthesis enzymes are
expressed in the veins of the vegetative tissues (Figure 1).
For example, ABA2 promoter analysis highlighted the
vessels [13], NCED3 expression has been associated with
xylem parenchyma cells [14], and AAO3 has been identi-
fied in both phloem companion cells and xylem parenchy-
ma cells [15]. NCED2, NCED3, and AAO3 are also present
in guard cells [15,16]. In seeds, ABA biosynthetic enzymes
have been found in both the maternal tissues and the
embryo [6,17–19]. Based on this, ABA synthesis is thought
to take place in the vasculature and in the guard cells of the
vegetative part of the plant; in seeds, all the tissues are
thought to be involved in ABA synthesis (Figure 1, red).
ABA plays a role in a range of physiological functions in
different plant tissues. During seed development, it first
helps to prevent viviparity and then contributes to dor-
mancy and desiccation tolerance, and counteracts the ac-
tion of other hormones, such as gibberellins [20]. ABA was
initially shown to originate first from maternal tissues and
then from the embryo only [20], but studies in Arabidopsis
have shown that zygotic tissues (endosperm and embryo)
play a role in both phases [19,21]. ABA in seedlings alters
their development, provoking the browning of cotyledons
and inhibiting root growth [22,23]. In the roots, exogenous-
ly applied ABA and studies using ABA-deficient mutants
indicate that ABA reshapes the root architecture by pre-
serving the growth of the primary root but inhibiting the
development of lateral roots at the checkpoint of meristem
activation [24–26]. These ABA effects in roots occur in the
meristem and elongation zones. In the leaf, ABA influences
growing tissues and has been extensively described in
guard cells, where it closes stomata [11,25]. The hydraulic
conductance of the leaf can also be reduced by ABA when
perfused from the petiole (i.e., with the vessels as the
primary site of action) [27]. ABA also plays a role in flowers,
where it could be involved in pollen dehiscence (see [28]
and references therein). From these examples, it is clear
that the accumulation of ABA in specific sites leads to
organ- or cell type-specific responses.
The physiological function of ABA and the localization of
its receptors are closely linked. There has been a long-
standing debate about the subcellular localization of ABA
Trends in Plant Science xx (2012) 1–9 1
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Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x

Seed

Leaf

Root

Em Mat

Ep Vasc St

P En C Ep
TRENDS in Plant Science

Figure 1. Schematic tissular localization of ABA synthesis, transport, and perception. Reporter-assay data from [13–19,23,32,55,57] and tissular gene expression data are
summarized to show the localization of ABA synthesis enzymes (red), ABA transporters (blue), and ABA receptors (green) in leaves (left panel), roots (middle panel), and
seeds (right panel). Genes involved in synthesis: NCED2, At4g18350; NCED3, At3g14440; NCED5, At1g30100; NCED6, At3g24220; NCED9, At1g78390; ABA2, At1g52340;
AAO3, At2g27150. Genes involved in transport: NRT1.2, At1g69850; AIT2, At1g27040; AIT3, At3g25260; AIT4, At3g25280; ABCG25, At1g71960; ABCG40, At1g15520. Genes
involved in perception: GTG1, At1g64990; GTG2, At4g27630; PYR1, At4g17870; PYL1, At5g46790; PYL2, At2g26040; PYL3, At1g73000; PYL4, At2g38310; PYL5, At5g05440;
PYL6, At2g40330; PYL7, At4g01026; PYL8, At5g53160; PYL9, At1g01360; PYL10, At4g27920; PYL11, At5g45860; PYL12, At5g45870; PYL13, At4g18620. Abbreviations: AAO,
aldehyde oxidase; ABA, abscisic acid; ABCG, ATP-binding cassette G; AIT, ABA-importing transporter; C, cortex; Em, embryo; En, endodermis; Ep, epidermis; GTG, GPCR-
type G protein; Mat, maternal tissues; NCED, 9-cis-epoxycarotenoid dioxygenases; NRT, nitrate transporter; P, pericycle; PYL, PYR1-like; PYR, pyrabactin resistance; St,
guard cells; Vasc, vascular tissues.

perception. Both intracellular and extracellular actions of
ABA have been published (e.g., [29,30]). Several proteins
[the RNA-binding protein FCA, Mg-chelatase H subunit
and G-protein-coupled receptor 2 (GCR2)] were initially
characterized as ABA receptors, but their exact nature or
role have not been confirmed [7]. Two membrane GPCR-
type G proteins (GTG1 and GTG2) were identified as ABA
receptors with an ABA binding site facing the apoplast
[22]. There are also noncontroversial intracellular recep-
tors that belong to the PYRABACTIN RESISTANCE 1
(PYR1)/PYR1-LIKE (PYL)/REGULATORY COMPO-
NENTS OF ABA RECEPTORS (RCAR) family [8]. The
expression of mRNA encoding these various receptors has
been observed in guard cells, vasculature, endosperm, and
embryos, according to data from the eFP browser website
(http://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi) [31], other
transcriptomic approaches (some are presented in
Figure 2) and promoter-reporter assays [32] (Figure 1,
green).
Historically, it has been assumed that ABA derived from
roots experiencing drought conditions would transit to the
2
xylem sap and reach elongating cells and guard cells to
prevent damage due to water loss and adapt the whole
plant to adverse conditions [33,34]. In this scenario, the
transport of ABA is unquestionable. However, recent stud-
ies have suggested that the distinction between sites of
synthesis and sites of perception is less clear-cut than
previously thought [35,36]. As summarized in Figure 1,
almost all cell types expressing ABA receptors are able to
synthesize the hormone, in particular veins, guard cells,
endosperm, and embryo. Thus, even though this view is
simplified and still incomplete, it raises questions about
the existence and need for ABA transport. A few argu-
ments confirm the existence of ABA transport across the
plasma membrane. First, ABA has been found in the xylem
sap. Because xylem vessels comprise dead cells and cannot
synthesize ABA, the presence of ABA indicates its trans-
port from another cell type. Second, there is evidence that a
significant proportion of ABA found in the roots is derived
from shoots [12,37,38], and a model of ABA transport has
been elaborated and is supported by experimental data
(Box 1). Third, it has long been known that cell membranes
TRPLSC-1043; No. of Pages 9
Review
are permeable to ABA (by diffusion and transporters, see
next paragraph). However, the existence of ABA transport
does not prove its adaptive or evolutionary benefits. For
example, a few reports over the past decade have chal-
lenged the need for root-sourced ABA in stomatal regula-
tion [35,39] and stomatal closure could be triggered only by
ABA synthesized in guard cells [15,16,40]. Such a hypoth-
esis has been recently confirmed upon exposure of plant
leaves to low relative humidity [36]. Finally, the molecular
cloning of ABA transporters and the phenotypes of their
respective mutants (see below) genetically supports the
requirement of ABA transport for its proper signaling
throughout the plant.
Two models for transmembrane ABA transport:
diffusion and transporters
Multiple studies of the biophysical properties and the phys-
iological effects of ABA in roots and leaves have progres-
sively lead to an ‘ionic trap model’, explaining the flux of
ABA between organs [33,41–46]. The biophysical aspects of
this model, based on the ability of protonated weak acids to
diffuse freely through the lipid bilayer, are presented in Box
1. In the case of ABA (pKa: 4.7), the pH of both cell and
apoplast implies that most of the ABA pools are in the ABA–,
charged and nondiffusible form. As a consequence, the
diffusion processes through the membrane are limiting
steps for ABA transport.
The topic of ABA transport was investigated in detail
during the 1970s. At that time, most of the flow of ABA
across membranes was assumed to occur as a result of
diffusion [47]. Evidence of a saturable transport (a signa-
ture of protein-mediated transport) was first presented in
1980 in specific regions of the root [48,49]. By the mid-
1990s, many tissues with saturable kinetics of ABA uptake
had been experimentally characterized [50–52]. The mo-
lecular bases of such transport were isolated 20 years later
and are presented below.
Box 1. Diffusion of weak acids and ‘ionic trap model’
A weak acid, such as ABA, is in equilibrium between the anionic (ABA–)
form and the protonated (ABA-H) form. This equilibrium is character-
ized by the pKa (4.7 for ABA), which is the pH at which both forms are at
the same concentration. This means that, at pH 4.7, 50% of abscisic acid
is in the ABA– form and 50% is in the ABA-H form. At a more acidic pH,
ABA-H is the dominant form; whereas at a basic pH [ABA–]>[ABA-H].
For example, at pH 7.7, [ABA–] = 1000  [ABA-H]. The protonated form
(ABA-H) is uncharged and, therefore, is able to diffuse freely through
the membrane lipid bilayer without the need of a transporter.
The biophysical properties and physiological effects of ABA in roots
and leaves have progressively led to an ‘ionic trap model’ that aims to
explain the flux of ABA between organs [33,41–46]. A simplified version
is presented here. ABA is synthesized primarily in vascular tissues and
will be dragged out by the flux of xylem sap. Apoplastic pH under
regular conditions ranges from 5.0 to 6.1, which implies that between
4% and 50% of apoplastic ABA is in the diffusible ABA-H form. On the
other side of the plasma membrane, at a cytoplasmic pH of 7.5, <0.2%
of ABA molecules are in the ABA-H, diffusible form. In resting
conditions, most of the apoplastic ABA-H molecules that cross the
membranes will therefore shift to the charged ABA– form. The cytosol is
thus in a constant ‘deficit’ with respect to the ABA-H form (i.e., it acts as
a trap). Given that the xylem sap is surrounded by vascular parenchyma
cells, bundle sheath cells, and mesophyll cells, it will be progressively
depleted of the hormone and it is likely that almost no ABA remains in
the xylem sap once it reaches the guard cells.
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
With respect to ABA uptake into cells, transporters
would allow better access of ABA to intracellular receptors
in the context of limited diffusion. Furthermore, the local-
ized expression of ABA transporters, and receptors, pro-
vides another level for controlling the activation of an ABA
signaling pathway in specific cell types only, as shown in
roots [53]. Finally, based on the ionic trap model, the major
biophysical issue in ABA transport across membranes
concerns the efflux. Efflux transporters would greatly en-
hance the loading of ABA into the xylem as well as in the
apoplast, therefore enabling a concentration to be reached
that could activate ABA signalization in other cells and
organs.
Molecular basis of ABA transport
Genetic screens that focused on auxin successfully led to
the identification of the different families of auxin trans-
porters as early as 1996 [54]; however, it was not until 2010
that two genetic screens finally allowed the cloning of ATP-
BINDING CASSETTE G25 and G40 (AtABCG25 and
AtABCG40) [23,55] as ABA transporters. Both proteins
belong to the large family of ABC transporter genes in
Arabidopsis [56]. Another recent study has led to the
identification of the nitrate transporter NRT1.2 as an
ABA transporter, which the authors of the study have
renamed ABA-IMPORTING TRANSPORTER 1 (AIT1)
[57]. However, NRT1.2 has already been characterized
as a nitrate (NO3–) transporter [58] and is a member of
the NRT1/PTR family [59].
AtABCG25 (At1g71960) and AtABCG40 (At1g15520)
were identified by their mutated forms in plants, from
screens of Ac/Ds insertion lines and a set of 15 ABC
mutants, respectively [23,55]. Their seed germination
showed an altered sensitivity to exogenous ABA. The
abcg22 mutant also exhibits a similar phenotype; however,
to date, ABA transport activity has not been demonstrated
for the corresponding protein [60]. NRT1.2 was identified
Environmental stresses, such as drought or N deprivation, increase
the pH of the xylem sap up to 6.7 [42,43], decreasing the pool of
apoplastic diffusible ABA-H to approximately 1%. If the cytosolic pH
and membrane properties are unchanged, the motive force for ABA-H
uptake and, therefore, its flow across the membrane, will be reduced
by 4 to 50. It is hypothesized that, under those conditions, the sap is
less depleted of ABA during its journey through plant tissues (and is
eventually enriched in ABA from the surrounding cells) and enough
hormone reaches the guard cells to induce stomatal closure. The role
of transporters with respect to this model is discussed in the main
text.
The model still holds many unsolved points. For example, the
consistency of the model in more complex setups, such as the partial
root-zone drying (PRD), where well-watered roots and roots
experiencing drought conditions exist together, still has to be
confirmed. An increase in xylem sap pH under PRD has been
documented [101], but was of low amplitude. The presence of ABA in
the leaf and its origin following PRD is still under investigation [102].
The model also has to fit alongside the role of ABA in the regulation
of shoot growth, given that it occurs in cells closer to vessels (i.e.,
earlier than guard cells with respect to the ionic trap). Finally, pH
regulation of ABA signaling acts in concert with other signaling
pathways, such as other chemical or electrical signals, miRNAs or
hydraulic processes, to regulate leaf homeostasis and function
during adverse conditions [25,35,103–105].
3
TRPLSC-1043; No. of Pages 9
Review
by using a screening system based on the ability of a
protein to transport ABA: a complementary DNA (cDNA)
library was screened in a yeast strain expressing the first
steps of the ABA transduction pathway split as a two-
hybrid system, comprising a PYR ABA-receptor, PYR1,
fused to the BETA-GALACTOSIDASE 4 (GAL4) activation
domain and type 2C protein phosphatase (PP2C), ABI1,
fused to the GAL4 DNA-binding domain. In the presence of
external ABA, expression of NRT1.2 allowed the entry of
ABA, which, in turn, promoted the binding of PYR–ABA to
the PP2C and restored the GAL4 transcription factor [57].
Three other members of the PTR family were also detected
in the same study: AIT2 (At1g27040), AIT3 (At3g25260),
and AIT4 (At3g25280). However, expression of the other
known ABA influx transporter, ABCG40, in this system did
not induce the ABA-dependent interaction between ABI1
and PYR1, demonstrating the limit of this screening meth-
od.
The ABA efflux activity of AtABCG25 was tested on
regenerated membrane vesicles from ABCG25-expressing
insect cells (Sf9 lines). As is typical for an ABC transporter,
this activity is ATP dependent [23]. With a Km of 260 nM,
AtABCG25 is a high-affinity transporter for the natural
enantiomer of ABA, (+)-ABA (or 10 S-(+)-ABA). Based on
loss-of-function mutants, it was shown that abcg25
mutants are more sensitive to externally applied ABA
during germination.
The ABA transport activity of AtABCG40 was tested by
heterologous expression in yeast and bright yellow 2 (BY2)
cells [55]. AtABCG40 is a high-affinity influx (+)-ABA
transporter with a Km of 1 mM. The affinity for ABA
obtained is usually higher in heterologous system than
in planta. Such a difference has been observed for other
transporters [61]. This could be explained by different ionic
environments, as well as by the lack of specific regulatory
proteins. abcg40-knockout mutant plants were less sensi-
tive to ABA for germination and lateral root development.
These knockout mutants were also less tolerant to drought
because of deficient ABA-induced stomatal closure. Inter-
estingly, guard cells of abcg40 were still sensitive to Ca2+-
induced stomatal closure, confirming that AtABCG40 acts
upstream of Ca2+ signaling and in accordance with a role in
ABA uptake.
The transport activity of NRT1.2 was tested by heterol-
ogous expression in yeast and Sf9 cells [57]. NRT1.2 has a
higher influx transport activity for (+)-ABA than for (–)-
ABA. A close homolog of NRT1.2, AIT3, was also tested in
yeast. AIT3 is also an ABA transporter, but it does not
discriminate between (+) and (–)-ABA. Furthermore it can
also transport gibberellin (GA3). The germination of the
nrt1.2 mutant plant was more sensitive to ABA inhibition,
and nrt1.2 mutants had lower inflorescence stem temper-
ature, which was related to an increased stem stomatal
aperture.
The cellular localization of the three transporters was
studied using the b-glucuronidase (GUS) reporter gene
under the control of AtABCG25, AtABCG40, or NRT1.2
promoters (Figure 1, blue). The AtABCG25 promoter is
active in the hypocotyl and in the vascular bundles of roots
and leaves [23]. The AtABCG40 promoter leads to a broad
expression pattern, with significant activity in guard cells
4
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
[55]. The NRT1.2 promoter is active in imbibed seeds and
vascular tissues; NRT1.2 is also expressed in epidermal
root cells and in root hairs [57]. Based on fusion proteins
with GFP, all three transporters were found to be localized
at the plasma membrane.
Altogether, these data suggest that AtABCG25 acts as
an efflux transporter that exports ABA out of the vessels,
AtABCG40 functions in the uptake of ABA into cells,
particularly guard cells, and NRT1.2 mediates the transfer
of ABA from the vessels to the other tissues in the inflo-
rescence [23,55,57].
The ABA transport activities of these three transporters
were tested in vitro at different pH levels: 7.0 for
AtABCG25 [23], 7.0 and 5.7 for AtABCG40 [55], and 7.5
for NRT1.2 [57]. Except for BY2 cells expressing
AtABCG40, no transport was assessed at the apoplastic
pH, which is known to be acidic [62]. Three questions
related to pH remain: (i) which ABA form is transported:
ABA– or ABA-H? (ii) Is H+ cotransported with ABA? And,
(iii) is the activity of the transporter regulated by pH?
Many questions are still unresolved and further work is
required to establish the physiological role of these trans-
porters, including their role during environmental stress
that increases the levels of endogenous ABA (as was
determined for AtABCG40).
Based on ABA physiological function, there are likely to
be other transporters at the sites of synthesis and percep-
tion of the hormone. Thus, future studies should include
seed maternal tissues, elongating cells in the root and
leaves, lateral root primordia, and inflorescences, and
should allow differentiation of the various cell types within
vessels. The physiological response of epidermal and me-
sophyll cells to ABA should also be analyzed with respect to
the expression of ABA transporters. Within the putative
new candidates (AtABCG22, AIT, and other close homo-
logs), the LATERAL ROOT-ORGAN DEFECTIVE/NU-
MEROUS INFECTIONS AND POLYPHENOLICS (latd/
nip) mutants from Medicago truncatula have a mutation in
PTR genes and exhibit a defect in primary root elongation,
probably because of an inactive meristem. Interestingly,
the application of ABA has a detrimental effect on wild
type roots, but has at first a beneficial effect on latd roots
[63]. In the same study, the authors tested ABA-induced
stomatal closure on latd mutants and found a loss of
sensitivity, which fits well with the hypothesis that LATD
could function as an ABA influx transporter [64].
Does NRT1.2 link N status to ABA signaling?
Many studies have linked NO3– and ABA signaling at the
physiological level. In seeds, high NO3– levels applied to
the mother plant or directly to the seed reduce dormancy
and decrease ABA content [65,66]. NO3– appears to act on
testa rupture and regulation of ABA and GA synthesis
enzymes [67]. In roots, aba and ABA-insensitive (abi)
mutants are less sensitive to the effects of NO3– on lateral
root development [26,68]. The loss of function of various
PTR in the latd/nip mutants in Medicago results in defects
in root development as well as in the arrest of nodule
formation: both of these processes are modulated by
ABA [25,26,69]. Primary root development can be partially
resumed by the application of exogenous ABA [63]. In
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Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x

leaves, guard cells are more sensitive to ABA upon NO3–
supply to the xylem sap [45]; however, this effect is lost if
the same experiment is carried out on epidermal peels only
[42]. This last result suggests that there is no direct
interaction between NO3– and ABA at the level of guard
cells, but such interplay could occur in mesophyll cells,
where the presence of NO3– would reduce ABA uptake by
mesophyll cells and let more ABA reach the apoplast of
guard cells. This hypothesis still has to be tested experi-
mentally.
Interestingly in this physiological context, most of the
plant NRT1/PTR members have been characterized as N-
containing molecule transporters, either in the form of
NO3–, amino acids, or dipeptides [70–72]. The ABA trans-
port capacity of NRT/PTR raises the possibility of a molec-
ular integration of N nutrition and ABA signaling into
single proteins. NRT1.2 is a perfect example because it
has already been isolated as an NO3– transporter [58]. Its
physiological role, as a root low-affinity NO3– transport
system, derives from its capacity to transport NO3– and
its localization in the epidermis. The role of NRT1.2 in ABA
signaling in stems comes from its capacity to transport ABA
and its localization in vessels. It is tempting to speculate
that NRT1.2, similar to its counterpart NRT1.1, could
function as a transceptor [73] involved in nitrate or ABA
sensing. So far, no phenotype associated with ABA trans-
port in the epidermis has been described, but NRT1.2 could
function in the import of ABA from the rhizosphere. We can
extrapolate that other NRT1/PTR, besides NRT1.2, are dual
transporters and act as logic gates for ABA and N signaling,
as has been shown for auxin and N [74,75]. We can also
speculate that, in the presence of a duality of transport, the
action of NRT1.2 or other NRT1/PTR in ABA signaling or
NO3– nutrition comes from their expression in specific cell
on
types. Those cell types could also express downstream
partners from one or the other function.
A transporter for conjugated ABA?
ABA conjugates define another class of molecules able to
shuttle the signal of ABA between organs [6,46,76]. In
particular, ABA-glucose ester (ABA-GE) is the most abun-
dant conjugated form of ABA and its level increases in
xylem sap upon drought stress [77]. The synthesis of ABA-
GE requires a glucosyl-transferase, whereas its dissocia-
tion to ABA requires b-glucosidases. Both types of enzyme
have been identified in plants [78–81], some being upre-
gulated in the context of environmental stresses. The
presence of b-glucosidase activity in the apoplast [78]
suggests that free ABA released from ABA-GE is available
at the outer face of the membrane, and mimics the acces-
sibility of the nonconjugated form of ABA. However, a
major b-glucosidase has been found in the cytosol [80]
and no glucosyl-transferase has been specifically identified
extracellularly. ABA-GE might therefore be synthesized
and/or perceived in the cytosol, which raises the question of
its transport across membranes, particularly given that
ABA-GE membrane permeabilities in resting conditions
appear to be low [50]. Thus, the existence of ABA-GE
transporters is possible. Such a role has been hypothesized
for an ABC transporter [76], and even tested for
AtABCG40 [55], but so far has not been established.
Transcriptional coordination of genes involved in the
triptych of ABA signaling
We analyzed the transcriptional regulation of genes in-
volved in the three steps of ABA signaling (synthesis,
transport, and perception) using data from published tran-
scriptomic experiments. The data sets were chosen to show

on
(a) (b)
rce ort

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Pe nsp is

Pe nsp is
p

p
s

s
Tra the

Tra the
Roots Shoots Roots Shoots
n

n
Sy

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PYL3: At1g73000 ABA2: At1g52340

NRT1.2: At1g69850 NCED9: At1g78390
PYL5: At5g05440 NCED6: At3g24220
ABCG25: At1g71960 7 PYL9: At1g01360
3 PYL9:
PYL4:
At1g01360
At2g38310
PYL2:
PYL7:
At2g26040
At4g01026
PYL6: At2g40330 PYL3: At1g73000
PYR1: At4g17870 AAO3: At2g27150
PYL1:
ABA2:
At5g46790
At1g52340
6 NCED3:
AIT4:
At3g14440
At3g25280
PYL2: At2g26040 NCED2: At4g18350
2
AIT2: At1g27040 NCED5: At1g30100
AIT3: At3g25260 AIT3: At3g25260
NCED9: At1g78390 * ABCG25: At1g71960
AIT4: At3g25280 AIT2: At1g27040
5
NCED5: At1g30100 * ABCG40: At1g15520
NCED6: At3g24220 * PYL6: At2g40330
1 AAO3:
ABCG40:
At2g27150
At1g15520
PYR1:
PYL4:
At4g17870
At2g38310
NCED2: At4g18350 * PYL5: At5g05440
4
NCED3: At3g14440 PYL1: At5g46790
PYL7: At4g01026 NRT1.2: At1g69850
PYL8: At5g53160 PYL8: At5g53160
Ct N S NS Ct N S NS Ct N S NS Ct N S NS *Low expression level W D W D
Light Dark
Dark Light Dark Relave expression level Relave expression level

–2.00 –0.21 2.00 –1.87 –0.21 2.00

TRENDS in Plant Science

Figure 2. Transcriptional coordination of genes involved in the synthesis, transport, and perception of ABA. Gene expression of genes involved in ABA synthesis, transport,
and perception have been clustered across two different data sets. (a) Response to nutritional cues: combination of NO3–, light, and sucrose treatments in two organs: roots
versus shoots (for more details, see supporting information in [100]). (b) Response to drought (D) as opposed to well-watered (W) treatment in roots versus shoots (GEO:
GSE40061 wild type samples have been used). The involvement of the genes in synthesis, transport, or perception is indicated by the red, blue, or green squares,
respectively. Only genes with an unambiguous probe on ATH1 chips were kept. The clustering of the results (numbered 1–7) led to two important conclusions: each gene is
preferentially expressed in roots or shoots with an over-representation of ABA-synthesis genes in shoots, and genes at every step of ABA signaling (synthesis, transport,
and perception) fit into ‘biomodules’ where they are coregulated (see also main text). Abbreviations: AAO, aldehyde oxidase; ABA, abscisic acid; ABCG, ATP-binding
cassette G; AIT, ABA-importing transporter; C, cortex; Ct, control; Em, embryo; En, endodermis; Ep, epidermis; GTG, GPCR-type G protein; Mat, maternal tissues; N, NO3–;
NCED, 9-cis-epoxycarotenoid dioxygenases; NRT, nitrate transporter; NS, NO3– and sucrose; P, pericycle; PYL, PYR1-like; PYR, pyrabactin resistance; S, sucrose; St, guard
cells; Vasc, vascular tissues.

5
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the root and shoot response separately to register potential
regulations that may be mediated at a particular organ
level. First, the signals being studied (i.e., nutritional and
drought) in the roots and shoots show a particular pattern
of expression and regulation (Figure 2). The most remark-
able feature appears to be that the synthesis-involved
genes tend to show (as a group) higher levels of expression
in shoots than in roots. Conversely, genes involved in
transport and perception tend to show higher levels of
expression in roots than in shoots. These observations
support the hypothesis that ABA may be produced pre-
dominantly in the shoots, transported away, and perceived
in the roots [35,37,38]. However, physiological regulations
may affect this overall static state of gene expression.
Indeed, several clusters appear if we examine gene regu-
lation by nutritional cues (Figure 2a). Cluster number 1
contains a group of shoot-expressed genes induced in dark
conditions. This cluster contains only one transporter,
most synthesis-involved genes and two receptors. In clus-
ter number 2, two genes (a synthesis-related gene and a
receptor) are induced upon light treatment in the shoot.
These two shoot-related clusters demonstrate that differ-
ent modules of regulation may coexist to adjust the overall
three-step ABA signaling pathway. The root-related clus-
ter number 3 (containing most perception-related genes) is
fairly insensitive to the nutritional cues applied in this
experiment (Figure 2a).
The analysis of the experiment reporting gene expres-
sion upon drought treatment leads to similar conclusions
(Figure 2b). Again, synthesis tends to be limited to shoot
parts. However, drought strongly regulates ABA-related
genes in roots. In cluster number 5, drought induces gene
expression. This induction is marked for receptor genes
and less pronounced for transporters. This behavior is
comparable with the shoot-related drought-induced cluster
number 6, which contains only synthesis and transport
genes. It is tempting to hypothesize that drought may
promote synthesis of ABA in shoots that is then trans-
ported to the root and perceived by cluster number 5 genes.
However, this hypothesis needs proper experimental vali-
dation. Interestingly, cluster number 7 is a shoot cluster
repressed by drought treatment and contains mainly per-
ception genes. It is tempting to speculate that drought
promotes ABA synthesis in shoots (through cluster number
6 genes) and that cluster number 7 is repressed to desen-
sitize the shoots to this locally produced ABA. However,
this will need proper experimental investigations to be
validated.
In conclusion, these examples of transcriptional regula-
tion demonstrate that each step of ABA signaling might be
involved in particular biomodules [82] under the influence
of an environmental signal. Available data enable a map of
gene regulation in shoots and roots to be sketched. The
identification of new molecular actors at each step of the
triptych may modify this picture, but some possible routes
of ABA synthesis, transport, and perception have already
been mapped out for the known players.
Specificity of transporters
ABC and NRT1/PTR transporters are present in all organ-
isms, but their respective families are larger in plants (for
6
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
example, humans have six PTR, yeast has one and Arabi-
dopsis has 53), suggesting that some of them have plant-
specific functions. This is somewhat confirmed by the
finding that both families contain plant hormone trans-
porters. Phylogenetic studies should identify the origin of
ABA transporters and examine the divergence between
ABA and indole-3 acetic acid transporters.
ABC transporters belong to a large protein family (130
members in Arabidopsis) and transport many different
molecules, such as mineral ions, lipids, metalloids, glyco-
sylated compounds, and hormones. They are localized on
different membranes (plasma membrane, tonoplast, per-
oxisome, chloroplast, and mitochondria), where they can be
involved in bidirectional transport. They have been exten-
sively reviewed elsewhere [83] and so will not be discussed
here. Nevertheless, bidirectional transport should be con-
sidered in future studies on ABA transport by ABC pro-
teins.
PTR belong to the SLC15 family [84], and are di- or
tripeptide transporters [85] capable of transporting pep-
tide-like drugs, such as b-lactam antibiotics. Unexpected-
ly, the first member of this family to be identified in a plant
was the nitrate transporter NRT1.1 [70]. Soon after, the
first plant dipeptide transporters were also identified in
this family [68,69]. Today, in addition to nitrate and pep-
tide transporters, this family includes: the histidine trans-
porter BnNRT1.2 [86], the auxin transporter AtNRT1.1
[74], the glucosinolate transporters GTR1 and GTR2 [87],
and the ABA transporters NRT1.2 and AIT3 [55]. We can
therefore assume that the spectrum of substrates that can
be transported by the NRT1/PTR family is far from com-
plete, raising the possibility that members of the NRT1/
PTR family have further physiological functions that have
yet to be determined, highlighting the need for functional
studies.
Both families (ABC and NRT1/PTR) have homologous
proteins that have been crystallized in other organisms
[88,89]. Some amino acids involved in the selectivity of
the transporters have been identified [88,89]. Structural
homology modeling should make it possible to hypothe-
size about whether the conserved regions (or amino
acids) that function for peptide transport are also used
by hormones (auxin for NRT1.1 or ABA for NRT1.2).
Following such an approach, structure–function analyses
should enable the identity of important amino acids to be
confirmed by expression in heterologous systems. Final-
ly, expression in plants of the mutated forms of the
transporters with altered selectivity should enable the
physiological consequences of a specific property to be
determined.
Concluding remarks
Retrospectively, it is astonishing that ABA transporters
have only been identified so recently, 20 years after the
first cloning of cDNAs encoding for ABA signal-transduc-
tion proteins [90,91]. Indeed, a similar delay has also been
observed for ABA receptors. The comparatively recent
isolation of transporters and receptors might either be
because they share redundant functions or because their
role is not significant enough for them to have been priori-
tized in earlier genetic screens.
TRPLSC-1043; No. of Pages 9
Review
Auxin fluxes in plant cells and tissues have been de-
scribed and modeled [92,93]. These models have benefited
from the characterization of auxin transporters, particu-
larly in terms of their cellular and subcellular localization
as well as their biophysical properties. Such models have
already been implemented for ABA [41], but will now
benefit from the identification of ABA transporters. In
addition to the generalized characterization methods
based on transcriptional data and reporter assays, it would
be of interest to focus on the protein itself in vivo, so as to
feed models with the most advanced functional data. Tools
for validation of modelization studies already exist: micro-
sampling and dosage or reporter genes have successfully
shown mobilization of pools of ABA in various parts of the
plant [40].
Finally, the presence and physiological activity of ABA
has been detected in other living organisms. Several groups
have reported the presence of ABA in humans [94–96], with
implications in inflammatory processes. The ABA signaling
paths experimentally tested so far include a plasma-mem-
brane receptor, G proteins, and their downstream events.
The presence of ABA in ferns and mosses is also well
documented, although the exact role of the hormone is still
controversial [97–99]. Furthermore, the molecular partners
of the signaling pathways, such as ABI3 transcription fac-
tors, PP2C, and SnRK2, are present in plants that diverged
more than 400 million years ago [11,97,98]. Future studies
should include the investigation of ABA transport and
transporters in those organisms because they may provide
new information about the coevolution of the transport of
ABA and other compounds, as well as an ABA signaling
network, between kingdoms.
Acknowledgments
We thank Antoine Martin and Jeffrey F. Harper for critical reading of the
manuscript. This work was supported by the Institut National de la
Recherche Agronomique (CJS PhD Fellowship to S.L.), Centre National
de la Recherche Scientifique (PEPS Bio-Math-Info-2012-2013-Super-
RegNet to G.K.), Agence Nationale de la Recherche (ANR-11-JSV6-002-
01-NUTSE to B.L. and ANR-11-PDOC-020-01-NITRONET to G.K.),
Agropolis Fondation (RHIZOPOLIS grant#07024 to A.G.), and the Région
Languedoc-Roussillon (Chercheur d’Avenir to B.L.).
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