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