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com

ScienceDirect
Long-distance transport of phytohormones through
the plant vascular system
Benoit Lacombe1 and Patrick Achard2
Phytohormones are a group of low abundance molecules that
activate various metabolic and developmental processes in
response to environmental and endogenous signals. Like
animal hormones, plant hormones often have distinct source
and target tissues, hence ensuring long-range communication
at the whole-plant level. Plants rely on various hormone
distribution mechanisms depending on the distance and the
direction of the transport. Here, we highlight the recent findings
on the long-distance movement of plant hormones within the
vasculature, from the physiological role to the molecular
mechanism of the transport.
Addresses
1
Biochimie et Physiologie Moleculaire des Plantes, UMR CNRS/INRA/
SupAgro/UM, Institut de Biologie Integrative des Plantes Claude
Grignon, 34060 Montpellier Cedex, France
2
Institut de biologie moleculaire des plantes, CNRS, Universite de
Strasbourg, 12 rue du General Zimmer, 67084 Strasbourg Cedex,
France
Corresponding author: Achard, Patrick (patrick.achard@ibmpcnrs.unistra.fr)

Current Opinion in Plant Biology 2016, 34:18

This review comes from a themed issue on Cell biology
Edited by Keiko Sugimoto and Arp Schnittger

http://dx.doi.org/10.1016/j.pbi.2016.06.007
1369-5266/# 2016 Elsevier Ltd. All rights reserved.

Introduction
Due to their sessile lifestyles, plants cannot escape from
adverse environmental situations such as drought, nutrient deficiency or pathogen attack. To overcome these
limitations, plants have evolved efficient mechanisms to
coordinate their growth and development with everchanging environmental conditions. Like all multicellular
organisms, this coordination requires communication mediated by signal molecules that move between the distal
organs of the plant. For example, root-derived signals
optimize shoot growth and adaptive responses under
dry soil conditions [1]. Studies examining the nature of
these signals revealed that classical phytohormones
such as auxin, abscisic acid, strigolactones, cytokinins,
gibberellins and jasmonates, participate in this long-distance communication system, ensuring spatio-temporal
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coordination of organ growth and development. Different

transport pathways orchestrate the translocation of these
molecules throughout the plant. Whereas auxin is essentially distributed in a given direction within tissue via a
unique cell-to-cell transport termed polar auxin transport (recently reviewed in [2]), the plant vascular system
is considered as the main route for long-distance transport
of the other phytohormones. During the last few years,
there has been considerable progress in term of our
understanding of this elaborate long-distance transport
system, including the characterization of hormone transporters (Table 1), using a range of non-invasive pharmacological methods associated with grafting techniques
to visualize hormone transport and distribution. In the
following paragraphs, we review some of the exciting
recent advances in long-distance hormone transport via
the plant vascular system.

The plant vascular system: a conduit for longrange communication

The vascular system plays a crucial role in plants in
providing both a mechanical support for aerial organs
and a conduit for long-distance transport of diverse molecules such as phytohormones [3]. The plant vascular
network is composed of two conductive tissues, xylem
and phloem, which transport molecules in largely opposite directions (Figure 1a). While xylem essentially transports water and nutrients from root to shoot, the phloem
distributes photosynthetic assimilates from source
(leaves) to sink tissues at the root and shoot apices. Xylem
vessels consist of tracheary elements, formed by thickwalled dead cells that connect various organs through the
entire plant body. In contrast, the phloem is composed of
living cells (sieve elements) depleted of most of their
organelles and nucleus, organized in sieve tubes associated with companion cells [3]. The organization of the
vascular system is different depending on the plant organ
[4]. Arabidopsis roots have a central xylem conduit
flanked by two phloem poles (Figure 1c), while stems
contain several vascular bundles consisting of phloem at
the periphery and xylem in the centre (Figure 1b).
In the past decade, our understanding of long-distance
communication system has greatly progressed and analysis of xylem and phloem exudates has provided clear
evidence that plant vascular network plays an essential
role in phytohormone distribution. It is noteworthy, however, that translocation of these molecules into or from
the vasculature also requires a transcellular radial transport, achieved by two different processes depending on
Current Opinion in Plant Biology 2016, 34:18

2 Cell biology

Table 1
Transporters involved in phytohormone transport and distribution mechanisms discussed in the review. See text for further details.
Name

Transporter family

Molecular function

ABCG25
ABCG30
ABCG31
ABCG40/PDR12
NPF4.1/AIT3
NPF4.2/AIT4
NPF4.5/AIT2
NPF4.6/AIT1
DTX50
PDR1
ABCG14
NPF2.10/GTR1
NPF3.1
LHT1

ABC
ABC
ABC
ABC
NPF
NPF
NPF
NPF
MATE
ABC
ABC
NPF
NPF
Amino acid carrier

ABA efflux
ABA influx
ABA efflux
ABA influx
ABA/GA influx
ABA influx
ABA influx
ABA influx
ABA efflux
SL efflux
CK efflux
GA/JA-Ile influx
GA/ABA influx
ACC influx

Spatial expression

References

Root, hypocotyl, leaf vasculature

Seeds
Seeds
Root, leaf, guard cells
n.d.
n.d.
n.d.
Seed, vascular tissues, stem
Seed, vascular tissues, guard cells
Root hypodermis, shoot axillary bud
Root stele, leaf vasculature, anther
Stamen filament, anther, pollen
Root endodermis
Root epidermis, leaf mesophyll

[17]
[19]
[19]
[16]
[18]
[18]
[18]
[18]
[20]
[30,31,32]
[48,49]
[57]
[59]
[80,81]

n.d., not determined.

Figure 1

(a)

(b)

stamen
GTR1

AIT1

Epidermis
Cortex
Endodermis

LHT1

Vascular bundle

ABCG
40

Procambium
Phloem

ABCG
14
DTX50

Xylem

ABCG
25

Pith
PDR1

Interfascicular region

(c)
ABCG
14

PDR1

Epidermis
Cortex
Endodermis
NPF3.1

Influx transporter

ABCG
25
LHT1

Efflux transporter
Phloem stream

Pericycle
Phloem
Xylem

Xylem stream

Current Opinion in Plant Biology

Schematic representation of vascular tissue organization in plants. (a) Routes of long-distance transport of phytohormones through the plant
vascular system. Xylem (red) and phloem (blue) translocate phytohormones from root to photosynthetic tissues and from source to sink tissues at
both apices, respectively. Hormone transporters described elsewhere in the article (see Table 1 for further details) are indicated with circles
colored in white for abscisic acid (ABA), blue for strigolactones (SLs), purple for cytokinins (CKs), green for gibberellins (GAs) and yellow for the
ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). The orientation of the transport is indicated by an arrow pointing inside (influx)
or outside (efflux) the circle symbol. (b,c) Schematic representation of stem (b) and root (c) cross-sections showing the organization of the
vascular tissues. The phloem is represented in blue and xylem in red.
Current Opinion in Plant Biology 2016, 34:18

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Long-distance transport plant hormones Lacombe and Achard 3

concentration gradient. Whereas hormones require the

function of active transporters to cross the plasma membrane in the direction against their concentration gradient, the uncharged forms of hormones (which increase at
acidic pH for carboxylated hormones such as ABA, jasmonic acid and gibberellins) can freely diffuse from
higher to lower concentrations (discussed for ABA in
[5]) and be trapped in the cell through ionic trap model
[6]. However, this biophysical model should not blind the
experimental approaches demonstrating that even in
these conditions, transporters are involved (Table 1).

Abscisic acid
Originally discovered in the early 1960s as a growth
inhibitor that accumulates during fruit abscission, abscisic
acid (ABA) is involved in manifold physiological processes, including seed germination, stomatal movement and
responses to environmental stresses [7,8]. In particular,
ABA is considered for long time as a hormonal stress
signal that moves throughout the plant to enhance resistance in distant organs [1]. Under mild drought stress, it is
widely accepted that ABA is accumulated in root tissues,
loaded into the xylem vessels, and transported shootward
by the transpiration stream where it acts on guard cells to
induce stomatal closure [9]. Moreover, recent data added
new levels of complexity to this model. First, guard cells
are autonomous for ABA synthesis in response to changes
in leaf hydration [10]. Secondly, ABA biosynthesis is also
highly induced in the vascular parenchyma cells upon
drought [11,12]. Last, accumulation of ABA content in
roots after long-term water stress largely relies on basipetal transport of ABA from aerial organs [13]. These
observations were confirmed with the ABA-specific optogenetic reporter that allows direct cellular monitoring
of dynamic ABA concentration changes in response to
environmental stresses [14,15]. Hence, further investigations will be crucial to provide clearer insights into
physiological roles of long-distance ABA transport in
response to drought.
At the molecular level, several ABA transporters have
been characterized [5,1620]: four G-type ATP-binding
cassette (ABC) transporters (ABCG25, 30, 31 and 40), four
NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER (NPF) proteins (NPF4.1/AIT3, NPF4.2/
AIT4, NPF4.5/AIT2 and NPF4.6/AIT1) and a DTX/
Multidrug and Toxic Compound Extrusion (MATE)
transporter (DTX50). Transporter activity studies performed in heterologous systems have shown that
ABCG25, ABCG31 and DTX50 act as ABA efflux transporters, while others function as ABA influx transporters.
Noteworthy, although the expression of most of these
transporters colocalizes to that of ABA biosynthesis genes
around vascular tissues, which is consistent with a function in long-distance ABA transport [5,11,12,1620], their
respective role in both acropetal and basipetal translocation of ABA is far from understood. Moreover, it cannot be
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ruled out that some of these transporters are also involved

in more local ABA movements such as in guard cells, as
proposed for NPF4.6/AIT1 [18]. Finally, it should be
noted that the glucose ester conjugated form of ABA
(ABA-GE) has been detected in xylem sap of various
plants and thus suggested to serve as long-distance transport form, but so far, the molecular identity of the carrier
remains to be established [5].

Strigolatones
Strigolactones (SLs) are carotenoid-derived molecules
that regulate various developmental responses, adapting
plant architecture to nutrient availability. SLs are exuded
from the roots into the soil to stimulate root colonization
by arbuscular mycorrhizal fungi, thereby enabling plants
to increase nutrient uptake from the rhizosphere [21].
Furthermore, SLs are transported from root to shoot to
inhibit lateral bud outgrowth [22]. Grafting experiments
showed that SLs are synthesized both in roots and shoots,
and that SL precursors are transported shootward in the
xylem to regulate shoot architecture [2225]. Hence,
whereas wild-type rootstocks are able to restore a wildtype development habit to grafted SL deficient scions,
wild-type shoots grafted on SL deficient rootstocks display a wild-type phenotype, indicating that shoots are
autonomous for SLs [2629]. Recently, it was demonstrated that PLEIOTROPIC DRUG RESISTANCE 1
(PDR1) from petunia, a G-type ABC transporter, has a
key role in releasing SLs from root producing cells, and
from vascular and nodal tissues surrounding axillary buds
[30,31]. PDR1 accumulates in shoot axils and is asymmetrically localized in root hypodermal cells, favoring
both acropetal transport of SLs and mycorrhizal fungi
entry [30,31]. Consistent with its function as a cellular SL
exporter, pdr1 mutants display lateral branching phenotype and they are defective in SL exudation in the soil,
thus resulting in reduced symbiotic associations [31]. To
date, except for its ortholog PDR6 in tobacco [32], no SL
transporters have been reported in other plant species.

Cytokinins
Cytokinins (CKs) are a group of mobile adenine derivatives involved in a plethora of biological processes including cell division and differentiation, apical dominance,
leaf senescence, root nodulation and nutrient homeostasis
[33]. Nitrate for example, stimulates the production of
trans-zeatin (tZ)-type CKs in the roots, which are then
translocated to the shoots by the xylem to modulate shoot
development [3439]. By contrast, N6-(D2-isopentenyl)
adenine (iP)-type CKs have been shown to move from
the shoots to the roots through the phloem to adjust
nitrogen acquisition [35,40,41], to regulate root nodulation [42], and to maintain vascular patterning in the root
meristem [43]. Chemical profiling associated with grafting experiments between CK biosynthesis mutants have
further demonstrated that both root-derived and shootderived CKs are respectively able to move acropetally and
Current Opinion in Plant Biology 2016, 34:18

4 Cell biology

basipetally through the plant vascular system [39,44]. At the

molecular level, previous in vitro work suggested that
members of the purine permease (PUP) [45] and equilibrative nucleoside transporter (ENT) families [46,47]
mediate CK translocation, but their involvement in the
long-distance CK transport in planta is unclear [34]. More
recently, two studies in Arabidopsis revealed that a G-type
ABC transporter, ABCG14, is essential for the long-distance transport of tZ-type CKs from the roots to the shoots
[48,49]. ABCG14 is expressed in stele cells in the root
differentiation zone, overlapping with CK production sites.
At the subcellular level, ABCG14 localizes at the plasma
membrane and likely functions as an efflux transporter
[48]. Loss of ABCG14 expression impairs tZ-type CK
accumulation in xylem sap and causes severe shoot growth
repression, a phenotype that is rescued by application of
exogenous CKs [48,49]. The role of ABCG14 for rootto-shoot translocation of CKs was further demonstrated
through grafting experiments. Whereas wild-type rootstocks are able to rescue the growth of abcg14 mutant scions,
wild-type scions grafted onto abcg14 rootstocks display
similar growth defect than abcg14 mutants [49]. By contrast, the basipetal transport of iP-type CKs is far less
understood and the transporters remain to be identified.

root, suggesting that functionally redundant GA transporters might compensate in the absence of NPF3.1
[59,61]. A second GA transporter, NPF2.10/GTR1,
has been shown to import bioactive GA3 in elongating
stamen filaments [57]. Accordingly, gtr1 mutants are
severely impaired in filament elongation and anther dehiscence, and application of exogenous GAs fully restores
the phenotype to that of the wild-type [57]. Remarkably,
GTR1 is also able to transport jasmonoyl-isoleucine (JAIle) into oocytes, a phytohormone also required for stamen development [57]. The contribution of GTR1 in
GA/JA interplay remains unclear. Last, NPF4.1/AIT3 has
been shown to import bioactive GAs in heterologous
system, but no function has been assigned to it [18].
The significance of GA transport in controlling growth
responses is not well understood, but it is assumed that
GAs provide an important communication system among
organs enabling adaptive growth throughout plant development. Consistent with this hypothesis, the transport of
GAs from photosynthetic source to sink organs has been
implicated in floral transition [62], and in the promotion of
internode elongation and secondary growth of the stem
[55,63], while root-to-shoot transport of GAs in DouglasFir has been shown to influence the timing of spring shoot
growth [64].

Gibberellins
Gibberellins (GAs) belong to a large family of diterpenoid
compounds that play essential role throughout plant
development, promoting seed germination, growth and
flowering [50,51]. Although GAs are mostly produced at
the site of action [50], numerous studies demonstrated
the existence of long-distance movements of endogenously made GAs, even though contradictory results were
obtained concerning the mobile form [5255,56]. While
studies in maize showed that bioactive GAs are transported [53], grafting experiments in pea indicated that
non-biologically active GA precursors are the mobile
forms [54]. Recently, micrografting experiments in Arabidopsis between hypocotyls of various GA-deficient
mutants provided clear evidence that the GA precursor
GA12 is the main mobile form, although this study cannot
rule out the possibility that other GAs can move locally in
plants [56]. Furthermore, quantitative analysis of endogenous GAs in xylem and phloem exudates indicated
that GA12 moves through the plant vascular system [56].
This, in turn, indicates that GAs conveyed in vascular
tissues must be translocated to specific tissues that require GAs for growth. Genetics and biochemical studies
allowed the identification of several GA transporters, all
belonging to the NPF family [18,57,58,59]. NPF3.1
encodes a plasma membrane influx transporter involved
in the accumulation of bioactive GAs into the root elongating endodermal cells, consistent with previous studies
showing that the endodermis is the main GA-responsive
tissue in the root [59,60]. Lack of NFP3.1 function in
npf3.1 mutants altered the distribution of fluorescentlylabeled bioactive GA4 in root but not the growth of the
Current Opinion in Plant Biology 2016, 34:18

Jasmonates
Jasmonates (JAs) are lipid-derived molecules (oxylipins)
that control specific developmental processes including
root elongation and fertility, and plant adaption to external challenges such as pathogens, insect herbivores and
wounding [65]. JAs are produced in response to tissue
damage and trigger both local and systemic defense
responses [66,67]. Hence, JAs were proposed to move
and operate at distance from their sites of synthesis.
However, although labeled JA feeding and grafting
experiments performed in Solanaceae were consistent
with long-distance transport of JAs [6870], studies in
Arabidopsis rather suggested the existence of a transmitted wound signal triggering systemic synthesis of JAs [66].
Recently, two studies provided clear evidence for both
wound-activated surface potential change (WASP) signal
and transport of endogenous JAs in plants [71,72]. First,
wounded leaves can communicate their damage status to
undamaged leaves by propagating electrical signals mediated by GLUTAMATE RECEPTOR-LIKE (GLR) genes
to stimulate distal JA production and signaling [71]. On
the other hand, wounded leaves produce JAs in xylem
contact cells that move radially from cell to cell and then
possibly over long-distance to undamaged tissues through
the plant vascular system [72,73]. Accordingly, micrografting experiments between hypocotyls of Arabidopsis
wild-type and JA-deficient mutants demonstrated the
existence of a basipetal transport of JAs, likely via the
phloem route [67,72]. Cotyledon-to-root translocation
of JA was further confirmed with the use of a fluorescent
JA biosensor [67]. Although JA and JA-Ile (the
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Long-distance transport plant hormones Lacombe and Achard 5

biologically active form) are abundant in many cells after

wounding and thus possible candidates for mobile signal,
it remains unclear which form of JA is mobile. Furthermore, except for NPF2.10/GTR1 [57] and few NPF
transporters identified in a modified yeast two-hybrid
system [58], the transporters involved in long-distance
translocation of JAs are still unknown.

Brassinosteroids and ethylene

Whereas long distance transport of the five above-described hormones has some molecular basis, far less
information has been obtained for brassinosteroids
(BRs). Indeed, despite the importance of this class of
steroid hormones for plant growth and their widespread
distribution in the plant, grafting and labeled BR feeding
experiments provided no evidence for long-distance
translocation of BRs [74,75]. By contrast, ethylene is a
gas that can freely diffuse from cell to cell, but also over
long distance through the aerenchyma or large intercellular voids [76]. The ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is also able to move
from root to shoot through the xylem, when the roots
are exposed to flooding or hypoxia [77,78]. Because ACC
is a non-protein amino acid, the role of amino acid carriers
in ACC transport has been hypothesized [79] and demonstrated recently. LYSINE-HISTINE TRANSPORTER
(LHT1) encodes an amino acid transporter taking part in
the transport of ACC [80,81].

Conclusion
Plants use their vascular system to distribute nutrients
and water throughout the plant body (minerals from root
to shoot and assimilates from shoot to root), but also to
transmit information signals between above-ground and
belowground tissues through the transport of phytohormones. Such long-distance hormone transport has been
thoroughly studied for decades via conventional grafting
and hormone feeding experiments. In the last few years,
the nature of the transmitted molecules has been identified, and may either involve the hormone itself, biosynthetic precursor (e.g. GA12), or conjugated form of the
hormone (e.g. ABA-GE). Furthermore, the molecular
identity of few hormone transporters has been revealed,
and they essentially fall in two protein families, the Gtype ABC and the NPF transporters (Table 1). Up to now,
each identified transporter has been characterized as
either an influx or efflux carrier, but since bidirectional
transporters have been identified in each family [82,83],
the directionality of these hormone transporters should be
reconsidered.
Finally, the presence of multisubstrate transporters highlights the next steps in the field. First, structure-function
analysis is needed to understand the molecular basis of
their selectivity: how NPF2.10/GTR1 could transport GA
and JA-Ile? Which amino acids in NPF2.10/GTR1 are
involved in the transport pathway? These questions can
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be answered by site directed mutagenesis but also using

structural approaches as done for NPF6.3 [84,85]. Second,
hormone crosstalk is important in many physiological and
developmental processes. Hence, the identification of
multihormone transporters is an important step forward
to understand and decipher these hormonal interconnections: for example, is NPF3.1 involved in GA/ABA antagonism or NPF2.10/GTR1 involved in GA/JA-Ile
crosstalk? Precise transport properties determined for
each substrate alone and in combination will probably
provide the clues to answer these questions.

Acknowledgements
We apologize to colleagues whose work could not be included owing to
space constraints. BL is financially supported by the Institut National de la
Recherche Agronomique (Projet Departement BAP, BAP2013-33-NITSE),
Agence Nationale de la Recherche (ANR-11-JSV6-002-01-NUTSE &
ANR-14-CE34-0007-01-HONIT) and the Region Languedoc-Roussillon
(Chercheur dAvenir), and PA acknowledges the Centre National de la
Recherche Scientifique.

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